systematic literature review and prisma

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How to Write a Systematic Review of the Literature

Affiliations.

1 1 Texas Tech University, Lubbock, TX, USA.
2 2 University of Florida, Gainesville, FL, USA.
PMID: 29283007
DOI: 10.1177/1937586717747384

This article provides a step-by-step approach to conducting and reporting systematic literature reviews (SLRs) in the domain of healthcare design and discusses some of the key quality issues associated with SLRs. SLR, as the name implies, is a systematic way of collecting, critically evaluating, integrating, and presenting findings from across multiple research studies on a research question or topic of interest. SLR provides a way to assess the quality level and magnitude of existing evidence on a question or topic of interest. It offers a broader and more accurate level of understanding than a traditional literature review. A systematic review adheres to standardized methodologies/guidelines in systematic searching, filtering, reviewing, critiquing, interpreting, synthesizing, and reporting of findings from multiple publications on a topic/domain of interest. The Cochrane Collaboration is the most well-known and widely respected global organization producing SLRs within the healthcare field and a standard to follow for any researcher seeking to write a transparent and methodologically sound SLR. Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA), like the Cochrane Collaboration, was created by an international network of health-based collaborators and provides the framework for SLR to ensure methodological rigor and quality. The PRISMA statement is an evidence-based guide consisting of a checklist and flowchart intended to be used as tools for authors seeking to write SLR and meta-analyses.

Keywords: evidence based design; healthcare design; systematic literature review.

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Open access
Published: 26 January 2021

PRISMA-S: an extension to the PRISMA Statement for Reporting Literature Searches in Systematic Reviews

Melissa L. Rethlefsen ORCID: orcid.org/0000-0001-5322-9368 1 ,
Shona Kirtley ORCID: orcid.org/0000-0002-7801-5777 2 ,
Siw Waffenschmidt ORCID: orcid.org/0000-0001-6860-6699 3 ,
Ana Patricia Ayala ORCID: orcid.org/0000-0002-3613-2270 4 ,
David Moher ORCID: orcid.org/0000-0003-2434-4206 5 ,
Matthew J. Page ORCID: orcid.org/0000-0002-4242-7526 6 ,
Jonathan B. Koffel ORCID: orcid.org/0000-0003-1723-5087 7 &

PRISMA-S Group

Systematic Reviews volume 10 , Article number: 39 ( 2021 ) Cite this article

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Literature searches underlie the foundations of systematic reviews and related review types. Yet, the literature searching component of systematic reviews and related review types is often poorly reported. Guidance for literature search reporting has been diverse, and, in many cases, does not offer enough detail to authors who need more specific information about reporting search methods and information sources in a clear, reproducible way. This document presents the PRISMA-S (Preferred Reporting Items for Systematic reviews and Meta-Analyses literature search extension) checklist, and explanation and elaboration.

The checklist was developed using a 3-stage Delphi survey process, followed by a consensus conference and public review process.

The final checklist includes 16 reporting items, each of which is detailed with exemplar reporting and rationale.

Conclusions

The intent of PRISMA-S is to complement the PRISMA Statement and its extensions by providing a checklist that could be used by interdisciplinary authors, editors, and peer reviewers to verify that each component of a search is completely reported and therefore reproducible.

Peer Review reports

Introduction

One crucial component of a systematic review is the literature search. The literature search, or information retrieval process, not only informs the results of a systematic review; it is the underlying process that establishes the data available for analysis. Additional components of the systematic review process such as screening, data extraction, and qualitative or quantitative synthesis procedures are dependent on the identification of eligible studies. As such, the literature search must be designed to be both robust and reproducible to ensure the minimization of bias.

Guidelines exist for both the conduct of literature searches (Table 2 ) for systematic reviews and their reporting [ 2 , 3 , 4 , 5 , 6 , 7 ]. Problematically, however, the many guidelines for reporting systematic review searches share few common reporting elements. In fact, Sampson et al. discovered that of the eleven instruments designed to help authors report literature searches well, only one item appeared in all eleven instruments [ 8 ]. Though Sampson et al.’s study was conducted in 2007, the problem has only been compounded as new checklists and tools have continued to be developed. The most commonly used reporting guidance for systematic reviews, which covers the literature search component, is the Preferred Reporting Items for Systematic reviews and Meta-Analyses Statement, or PRISMA Statement [ 9 ]. The 2009 PRISMA Statement checklist included three items related to literature search reporting, items 7, 8, and 17:

Item 7: Describe all information sources (e.g., databases with dates of coverage, contact with study authors to identify additional studies) in the search and date last searched.

Item 8: Present full electronic search strategy for at least one database, including any limits used, such that it could be repeated.

Item 17: Give numbers of studies screened, assessed for eligibility, and included in the review, with reasons for exclusions at each stage, ideally with a flow diagram.

Despite wide usage of the PRISMA Statement [ 10 ], compliance with its items regarding literature search reporting is low [ 11 , 12 , 13 , 14 ]. Even for those studies which explicitly reference PRISMA, there is only slight, statistically non-significant evidence of improved reporting, as found by Page et al. [ 15 ]. Part of the challenge may be the multifactorial nature of each of the PRISMA items relating to searches; authors may feel if they completed one of the components of the item that they can check off that item altogether. Another part of the challenge may be that many systematic reviews do not include librarians or information specialists as members of the systematic review team or as authors on the final manuscript [ 11 , 16 , 17 , 18 ]. Preliminary research suggests that librarian or information specialist involvement is correlated with reproducibility of searches [ 16 , 17 , 18 ], likely due to their expertise surrounding search development and documentation. However, reviews where librarians are authors still include reproducible searches only 64% of the time [ 17 ].

A larger issue may be that, even amongst librarians and information specialists, debate exists as to what constitutes a reproducible search and how best to report the details of the search. Researchers assessing the reproducibility of the search have used varying methods to determine what constitutes a reproducible search [ 11 , 17 , 19 , 20 ]. Post-publication peer review of search methods, even amongst Cochrane reviews, which generally have superior reporting compared to non-Cochrane reviews [ 15 ], has shown that reporting that appears complete may still pose challenges for those wishing to reproduce searches [ 20 , 21 , 22 , 23 , 24 ]. Furthermore, little guidance on how to report searches using information sources or methods other than literature databases, such as searching web sites or study registries, exists [ 25 , 26 ].

Incomplete reporting of the literature search methods can introduce doubt and diminish trust in the final systematic review conclusions. If researchers are unable to understand or reproduce how information was gathered for a systematic review, they may suspect the authors of having introduced bias into their review by not conducting a thorough or pre-specified literature search. After observing the high number of systematic reviews with poorly reported literature searches, we sought to create an extension to the PRISMA statement. Our aims were four-fold:

To provide extensive guidance on reporting the literature search components of a systematic review.

To create a checklist that could be used by authors, editors, and peer reviewers to verify that each component of a search was completely reported and therefore reproducible.

To develop an interdisciplinary checklist applicable to all method-driven literature searches for evidence synthesis.

To complement the PRISMA Statement and its extensions.

Because we intend the checklist to be used in all fields and disciplines, we use “systematic reviews” throughout this document as a representative name for the entire family of evidence syntheses [ 27 ]. This includes, but is not limited to, scoping reviews, rapid reviews, realist reviews, metanarrative reviews, mixed methods reviews, umbrella reviews, and evidence maps [ 28 ]. We use the term “literature search” or “search” throughout to encompass the full range of possible search methods and information sources.

Part 1: Developing the Checklist

After consultation with members of the PRISMA Statement steering group (D.M. and D.G.A.), we formed an executive committee (M.L.R, J.K., S.K.) and developed a protocol [ 29 ] according to the steps outlined in the “Guidance for Developers of Health Research Reporting Guidelines [ 30 ].” The protocol was registered on the EQUATOR Network [ 29 ]. We identified 405 potential items relevant to reporting searches in systematic reviews from 61 sources (see Additional file 1 ) located through a search of MEDLINE via Ovid, Embase via Embase.com , and LISTA via EBSCOhost, in addition to reviewing all of the sources identified by the EQUATOR Network relating to systematic reviews. We also searched our personal files and examined references of included documents for additional sources. Details of the search are available in Additional file 1 . Sources included both explicit reporting guidelines and studies assessing reproducibility of search strategies. The 405 items were reviewed for overlap and consolidated into 123 remaining items for potential inclusion in a checklist.

To narrow the list into a usable checklist, we then used a three-step Delphi survey process [ 31 ]. The first survey included the initially identified 123 items and asked respondents to rate each item on a 4-point Likert-type scale. Items that 70% of experts rated as 3 or 4 (4 being “essential” and 1 “not important”) and that received a mean score of at least 3.25 were retained for rating in the second round of the Delphi process. Respondents to the first survey were invited to participate in the second and third rounds. The second round asked respondents to pick the 25 most essential items out of the remaining 53 potential items; the third round was identical, except respondents also selected the most appropriate location for reporting their selected items (e.g., in the main text, or a supplementary file). The items were ranked and categorized by general theme for discussion at an in-person consensus conference.

We created a list of one hundred and sixty-three international experts, including librarian and information specialists with expertise in systematic reviews, researchers who had written about systematic review reporting, journal editors, and systematic review methodologists, to whom we sent our initial Delphi survey. The list of experts was created using a combination of publications, mailing lists, conference proceedings, and knowledge of the authors to represent research groups and experts in 23 countries. We received 52 responses (32% response rate) to the first survey, and of these, 35 (67% response rate) completed both surveys two and three. This study was declared exempt by the University of Utah Institutional Review Board (IRB_00088425).

The results of the Delphi process were reported at a consensus conference meeting that took place in May 2016 concurrently with Mosaic ‘16, the joint meeting of the Medical Library Association, Canadian Health Libraries Association/Association des bibliothèques de la santé du Canada, and the International Clinical Librarian Conference (ICLC). 38 individuals attended the consensus conference, 14 (37%) of whom had participated in the Delphi surveys. At the consensus conference, the grouped and ranked remaining items were distributed to small groups who were asked to discuss, consolidate, remove, or add missing critical items under the guidance of a group leader. After two rounds of discussion, the group leaders presented the discussion and proposed list items from their small groups for consideration by the whole group of experts.

Upon completion of the consensus conference, 30 items remained from those identified during the Delphi process, with an additional three items that had been excluded during the Delphi process added back to the draft checklist because meeting attendees considered them critical to the guideline. The list was then consolidated and reviewed by executive committee members, including two new information specialist members (S.W. and A.P.A). The draft checklist and explanation and elaboration document was released to the public on March 20, 2019, along with all data and study materials [ 32 ]. All participants in the Delphi process and/or consensus conference were contacted via email with instructions on how to provide feedback on the draft checklist items and/or elaboration and explanation document by commenting directly on the explanation and elaboration draft using a private commenting system, Hypothesis [ 33 ], or if preferred, via email. Comments from other interested individuals were solicited via Twitter, conference presentations, and personal contacts. Comments were collected from the private Hypothesis group, the public Hypothesis comments, and via email. All comments were combined into a single document. Executive committee members reviewed each comment in duplicate to indicate what type of feedback was received (i.e., linguistic, major substantive, minor substantive, or unclear) and, for substantive comments, whether change was recommended or required further discussion.

During the draft and revision process (March 20–June 15, 2019), 358 separate comments were received from 22 individuals and organizations. Based upon the extensive feedback received, the executive team revised the checklist and developed the next iteration, which was released on December 6, 2019, to coincide with the 2019 Virtual Cochrane Colloquium Santiago. Additional feedback from this release was incorporated into the final checklist. Throughout the draft and revision process, several teleconferences were held with the lead of the PRISMA 2020 statement (M.J.P), as an update of the 2009 PRISMA statement was in development, to ensure that the content on search methods was consistent between the PRISMA 2020 and PRISMA-S guidelines [ 34 , 35 ].

Part 2: Checklist

PRISMA-S is a 16-item checklist that covers multiple aspects of the search process for systematic reviews. It is intended to guide reporting, not conduct, of the search. The checklist should be read in conjunction with the Explanation and Elaboration (Part 3), which provides more detail about each item. We also include two boxes, one a glossary of terms (see Table 2 ) and the other, guidance on depositing search data and method descriptions in online repositories (see Table 3 ).

The Explanation and Elaboration also includes examples of good reporting for each item. Each exemplar is drawn from published systematic reviews. For clarity, some exemplars are edited to match the style of this document, including any original citations, and abbreviations are spelled out to aid comprehension. Any other edits to the text are noted with square brackets. A description of the rationale behind the item is explained, followed by additional suggestions for clear reporting and a suggested location(s) for reporting the item.

Not every systematic review will make use of all of the items in the Information Sources and Methods section of the checklist, depending on the research question and the methods chosen by the authors. The checklist provides a framework for the current most common and recommended types of information sources and methods for systematic reviews, but authors should use and report those items relevant and appropriate to their review. The checklist may also be used for systematic review protocols to fully document the planned search, in conjunction with the PRISMA-P reporting guideline [ 36 ] (Table 1 ).

Part 3: Explanation and Elaboration

Item 1. database name.

Name each individual database searched, stating the platform for each.

“The following electronic databases were searched: MEDLINE (Ovid), CINAHL (EBSCOhost), PsycINFO (Ovid), Cochrane Central Register of Controlled Trials (Ovid), SPORTDiscus (EBSCOhost), EMBASE (Ovid) and ProQuest Dissertations and Theses Global (ProQuest).” [ 38 ]

Explanation

Databases are the most commonly used tool to locate studies to include in systematic reviews and meta-analyses [ 6 , 39 ]. There is no single database that is able to provide a complete and accurate list of all studies that meet systematic review criteria due to the differences in the articles included and the indexing methods used between databases (Table 2 ). These differences have led to recommendations that systematic review teams search multiple databases to maximize the likelihood of finding relevant studies [ 6 , 39 , 40 ]. This may include using broad disciplinary databases (e.g., MEDLINE [ 41 ], Embase [ 42 ], Scopus [ 43 ]), specialized databases (e.g., PsycINFO [ 44 ] or EconLit [ 45 ]), or regional databases (e.g., LILACS [ 46 ] or African Index Medicus [ 47 ]).

Many of these literature databases are available through multiple different search platforms (Table 2 ). For example, the MEDLINE database is available through at least 10 different platforms, including Ovid, EBSCOhost, Web of Science, and PubMed. Each platform offers different ways of searching the databases, such as platform-specific field codes (Table 2 ), phrase searching, truncation, or searching full-text versus abstract and keyword only [ 48 ]. Different platforms may contain additional data that are not available in the original database, such as times cited, social media impact, or additional keywords. These differences between the platforms can have a meaningful impact on the results provided [ 48 , 49 , 50 ].

Authors should identify which specific literature databases were searched to locate studies included in the systematic review. It is important that authors indicate not only the database, but the platform through which the database was searched. This helps readers to evaluate the quality and comprehensiveness of the search and supports reproducibility and updating (Table 2 ) in the future by allowing the strategy to be copied and pasted as recommended in Item 8, below.

The distinctions between database and platform may not always be clear to authors, especially when the database is the only one available through a platform (e.g., Scopus [ 43 ]). In these cases, authors may choose to include the web address of the database in the text or the bibliography to provide clarity for their readers.

Suggested location for reporting

Report each database name and platform in the methods section and any supplementary materials (Table 2 ). If space permits, report key database names in the abstract.

Item 2. Multi-database searching

If databases were searched simultaneously on a single platform, state the name of the platform, listing all of the databases searched.

“The MEDLINE and Embase strategies were run simultaneously as a multi-file search in Ovid and the results de-duplicated using the Ovid de-duplication tool.” [ 51 ]

“A systematic literature search was performed in Web of Knowledge™ (including KCI Korean Journal Database, MEDLINE, Russian Science Citation Index, and SciELO Citation Index)….” [ 52 ]

Authors may choose to search multiple databases at once through a single search platform to increase efficiency. Along with the name of the platform, it is necessary to list the names of each of the individual databases included as part of the search. Including information about using this approach in the text of the manuscript helps readers immediately understand how the search was constructed and executed. This helps readers determine how effective the search strategy (Table 2 ) will be for each database [ 1 ].

Report any multi-database search (Table 2 ) in the methods section and any supplementary materials. If space permits, report key individual database names in the abstract, even if run through a multi-database search.

Item 3. Study registries

List any study registries searched.

“[We] searched several clinical trial registries ( ClinicalTrials.gov , Current Controlled Trials ( www.controlled-trials.com ), Australian New Zealand Clinical Trials Registry ( www.actr.org.au ), and University Hospital Medical Information Network Clinical Trials Registry ( www.umin.ac.jp/ctr )) to identify ongoing trials.” [ 53 ]

Study registries are a key source of information for systematic reviews and meta-analyses in the health sciences and increasingly in other disciplines. In the health sciences, study registries (Table 2 ) allow researchers to locate ongoing clinical trials and studies that may have gone unpublished [ 54 , 55 , 56 ]. Some funders, including the National Institutes of Health, require principal investigators to share their data on study registries within a certain time frame after grant completion [ 57 ]. This data may not have been published in any other location, making study registries a critical component of an information strategy, though timely reporting remains a challenge [ 58 , 59 ]. Different countries have their own study registries, as do many pharmaceutical companies.

Outside the health sciences, study registries are becoming increasingly important as many disciplines adopt study pre-registration as a tactic for improving the rigor of research. Though not yet as established as in the health sciences, these study registries are continually expanding and will serve as key sources for finding unpublished studies in fields in the social sciences and beyond.

To fully describe the study registries searched, list the name of each study registry searched, and include a citation or link to the study registry.

Report any study registries searched in the methods section and any supplementary materials.

Item 4. Online resources and browsing

Describe any online or print source purposefully searched or browsed (e.g., tables of contents, print conference proceedings, web sites), and how this was done.

“ We also searched the grey literature using the search string: “public attitudes” AND “sharing” AND “health data” on Google (in June 2017). The first 20 results were selected and screened.” [ 60 ]

“The grey literature search was conducted in October 2015 and included targeted, iterative hand searching of 22 government and/or research organization websites that were suggested during the expert consultation and are listed in S1 Protocol. Twenty two additional citations were added to the review from the grey literature search.” [ 61 ]

“To locate unpublished studies, we searched Embase [via Embase.com ] for conference proceedings since 2000 and hand-searched meeting abstracts of the Canadian Conference on Physician Health and the International Conference on Physician Health (2012 to 2016).” [ 62 ]

Systematic reviews were developed to remove as much bias as possible from the literature review process. One of the most important ways they achieve this reduction in bias is by searching beyond literature databases, which are skewed towards English-language publications with positive results [ 63 , 64 ]. To achieve a fuller picture of what the research on a specific topic looks like, systematic reviewers could seek out research that may be in progress and research that was never published [ 6 ]. Using other methods of finding research also helps identify research that may have been indexed in literature databases, but went undiscovered when searching those sources [ 40 ]. Seeking out this research often involves a complex strategy, drawing on a wealth of online and print resources as well as personal contacts.

Web search engines and specific web sites

Searching general internet search engines and searching the contents of specific websites is a key component of many systematic reviews [ 26 , 65 ]. Government, non-profit organization, and pharmaceutical company websites, for example, contain a wealth of information not published elsewhere [ 6 , 66 ]. Though searching a general search engine like Google or using a general search engine to search a specific website may introduce some bias into the search methodology through the personalization algorithms inherent in many of these tools [ 67 , 68 ], it is still important to fully document how web searches were conducted [ 65 ].

Authors should list all websites searched, along with their corresponding web address. Readers should be able to clearly understand if researchers used a website’s native search interface or advanced search techniques within a general search engine. If authors used a general search engine, authors should declare whether steps were taken to reduce personalization bias (e.g., using “incognito” mode in a browser). Authors may choose whether to detail the websites searched within the text (i.e., Google ( http://www.google.com )), by citing the websites in the bibliography, or by listing the website with corresponding web address in supplementary material, as shown in the examples above.

Review teams may occasionally set an artificial limit to the number of items they will screen from a given search or source [ 65 ]. This is because searching web search engines and individual websites will often lead to an unmanageable number of results, the search engine itself may only display a restricted number of results (e.g., Google will only display 1000 results), or the team has a finite budget or timeline to complete the review. Thus, many systematic review teams utilizing web search engines will often pre-designate a limit to the number of results they review. If review teams choose to review a limited set of results, it should be noted in the text, along with the rationale.

Conference proceedings

Studies show that large percentages of research presented as papers and posters at conferences never make their way into the published literature, particularly if the study’s results were statistically negative [ 63 , 69 ]. Conference proceedings are often the only way to locate these studies. Including conference proceedings in a systematic review search helps minimize bias [ 70 ]. The introduction of online conference proceedings has been a boon to researchers and reduced the need to review printed abstract books. Additionally, some databases either include conference proceedings along with journal articles (i.e., Embase [ 42 ]) or contain only conference proceedings (i.e., ProceedingsFirst [ 71 ] or Directory of Published Papers [ 72 ]). Some conferences have made their abstracts available in a single database (i.e., International AIDS Society’s Abstract Archive [ 73 ]). When using these types of databases to search conference proceedings, authors can treat them as above in Item 1.

Individual conferences’ online proceedings may be password-protected for association members or conference attendees [ 74 ]. When reporting on conference proceedings searched or browsed (Table 2 ) via a conference or association’s online or print proceedings, authors must specify the conference names, the dates of conferences included, and the method used to search the proceedings (i.e., browsing print abstract books or using an online source). If the conference proceedings are searched online, authors should specify the web address(es) for the conference proceedings and the date(s) of the conferences. If the conference proceedings are published in a journal, the authors should cite the journal. If the proceedings are a standalone publication, authors may choose to cite them using the same methods used to cite a book or by providing the full information about the conference (name, location, dates, etc.) in a supplementary file.

General browsing

Authors also commonly browse print or online tables of contents, full contents of journals, or other sources that are the most likely to contain research on the topic sought. When purposefully browsing, describe any method used, the name of the journal or other source, and the time frame covered by the search, if applicable.

Report online information sources (Table 2 ) searched or browsed in the methods section and in any supplementary materials. Systematic reviews using several of these methods, or using multiple information sources for each method, may need to report their methods briefly in the methods section, but should fully report all necessary information to describe their approaches in supplementary materials.

Item 5. Citation searching

Indicate whether cited references or citing references were examined, and describe any methods used for locating cited/citing references (e.g., browsing reference lists, using a citation index, setting up email alerts for references citing included studies).

“Reference lists of included articles were manually screened to identify additional studies.” [ 75 ]

“[W]e used all shared decision making measurement instruments that were identified in Gärtner et al’s recent systematic review (Appendix A). We then performed a systematic citation search, collecting all articles that cited the original papers reporting on the development, validation, or translation of any the observational and/or self-reported shared decision making measurement instruments identified in that review. An experienced librarian (P.J.E.) searched Web of Science [Science Citation Index] and Scopus for articles published between January 2012 and February 2018.” [ 76 ]

“We [conducted] citation tracking of included studies in Web of Science Core Collection on an ongoing basis, using citation alerts in Web of Science Core Collection.” [ 77 ]

One of the most common search methods is reviewing the references or bibliographies of included studies [ 11 , 17 ]. This type of citation searching (looking for cited references) can be additive to other cited reference searching methods, such as examining bibliographies of relevant systematic reviews. In addition, researchers may choose to look for articles that cite specified studies [ 78 ]. This may include looking beyond one level forwards and backwards (e.g., examining the bibliographies of articles cited by specified articles) [ 78 ]. Looking at bibliographies of included articles or other specified articles is often conducted by examining full-text articles, but it can also be accomplished using online tools called citation indexes (Table 2 ).

The use of these methods can be complicated to describe, but the explanation should clearly state the database used, if applicable (i.e., Scopus, Google Scholar, Science Citation Index) and describe any other methods used. Authors also must cite the “base” article(s) that citation searching was performed upon, either for examining cited or citing articles (Table 2 ). If the same database is used for both a topical search as well as citation searching, describe each use separately. For manually checking the reference lists for included articles, a simple statement as in the first example is sufficient.

Report citation searching details in the methods section and in any supplementary materials.

Item 6. Contacts

Indicate whether additional studies or data were sought by contacting authors, experts, manufacturers, or others.

“We contacted representatives from the manufacturers of erythropoietin-receptor agonists (Amgen, Ortho-Biotech, Roche), corresponding or first authors of all included trials and subject-area experts for information about ongoing studies.” [ 79 ]

“We also sought data via expert requests. We requested data on the epidemiology of injecting drug use and blood-borne viruses in October, 2016, via an email distribution process and social media. This process consisted of initial emails sent to more than 2000 key experts and organisations, including contacts in the global, regional, and country offices of WHO, UNAIDS, Global Fund, and UNODC (appendix p 61). Staff in those agencies also forwarded the request to their colleagues and other relevant contacts. One member of the research team (SL) posted a request for data on Twitter, which was delivered to 5525 individual feeds (appendix p 62).” [ 80 ]

Contacting manufacturers (e.g., pharmaceutical companies), or reaching out to authors or experts directly or through organizations, is a key method to locate unpublished and ongoing studies [ 6 ]. Contacting authors or manufacturers may also be necessary when publications, conference proceedings, or clinical trials registry records do not provide the complete information needed [ 63 , 81 ]. Contacting manufacturers or regulating agencies might be required to acquire complete trial data from the clinical study reports [ 82 , 83 ]. More broad calls for evidence may also be conducted when no specific groups or individuals are targeted.

Contact methods may vary widely, depending on the context, and may include personal contact, web forms, email mailing lists, mailed letters, social media contacts, or other methods. As these strategies are inherently difficult to reproduce, researchers should attempt to give as much detail as possible on what data or information was sought, who or what group(s) provided data or information, and how the individuals or groups were identified.

Report information about contacts to solicit additional information in the methods section and in any supplementary materials. Systematic reviews using elaborate calls for evidence or making extensive use of contacts as an information source may need to report their methods briefly in the methods section, but should fully report all necessary information to describe their approaches in supplementary materials.

Item 7. Other methods

Describe any additional information sources or search methods used.

“We also searched… our personal files.” [ 84 ]

“PubMed’s related articles search was performed on all included articles.” [ 85 ]

A thorough systematic review may utilize many additional methods of locating studies beyond database searching, many of which may not be reproducible methods. A key example is searching personal files. Another is using databases’ built in tools, such as PubMed’s Related Articles feature [ 86 ] or Clarivate Analytics’ Web of Science’s Related Records feature [ 87 ], to locate relevant articles based on commonalities with a starting article. Because these tools are often proprietary and their algorithms opaque, researchers may not be able to replicate the exact results at a later date. To attempt to be as transparent as possible, researchers should both note the tool that was used and cite any articles these operations were run upon. For all “other” methods, it is still important to declare that the method was used, even if it may not be fully replicable.

Report information about any other additional information sources or search methods used in the methods section and in any supplementary materials.

Item 8. Full search strategies

Include the search strategies for each database and information source, copied and pasted exactly as run.

Database search. Methods section description . “The reproducible searches for all databases are available at DOI:10.7302/Z2VH5M1H.” [ 88 ]

Database search. One of the full search strategies from supplemental materials in online repository . “ Embase.com (692 on Jan 19, 2017) 1. 'social media'/exp OR (social NEAR/2 (media* OR medium* OR network*)):ti OR twitter:ti OR youtube:ti OR facebook:ti OR linkedin:ti OR pinterest:ti OR microblog*:ti OR blog:ti OR blogging:ti OR tweeting:ti OR 'web 2.0':ti 2. 'professionalism'/exp OR 'ethics'/exp OR 'professional standard'/de OR 'professional misconduct'/de OR ethic*:ab,ti OR unprofessional*:ab,ti OR professionalism:ab,ti OR (professional* NEAR/3 (standard* OR misconduct)):ab,ti OR ((professional OR responsib*) NEAR/3 (behavi* OR act OR conduct*)):ab,ti 3. #1 AND #2 AND [english]/lim NOT ('conference abstract':it OR 'conference paper':it) [ 88 ]

Online resources and browsing. Methods section description . “The approach to study identification from this systematic review is transparently reported in the Electronic Supplementary Material Appendix S1.” [ 89 ]

Online resources and browsing. One of the full online resource search strategies reported in supplement . “Date: 12/01/16. Portal/URL: Google. https://www.google.co.uk/webhp?hl=en . Search terms: ((Physical training) and (man or men or male or males) and (female or females or women or woman) and (military)). Notes: First 5 pages screened on title (n=50 records).” [ 89 ]

Systematic reviews and related review types rely on thorough and complex search strategies to identify literature on a given topic. The search strategies used to conduct this data gathering are essential to the transparency and reproducibility of any systematic review. Without being able to assess the quality of the search strategies used, readers are unable to assess the quality of the systematic review [ 9 , 11 , 17 ].

When space was at a premium in publications, complete reporting of search strategies was a challenge. Because it was necessary to balance the need for transparency with publication restrictions, previous PRISMA guidelines recommended including the complete search strategy from a minimum of one database searched [ 9 ]. Many systematic reviews therefore reported only the minimum necessary. However, reporting only selected search strategies can contribute to the observed irreproducibility of many systematic reviews [ 11 , 17 ].

The prior versions of PRISMA did not elaborate on methods for reporting search strategies outside of literature databases. Subsequent to its publication, many groups have begun identifying the challenges of fully documenting other types of search methods [ 90 , 91 ]. Now recommended is the explicit documentation of all of the details of all search strategies undertaken [ 91 , 92 ]. These should be reported to ensure transparency and maximum reproducibility, including searches and purposeful browsing activities undertaken in web search engines, websites, conference proceeding databases, electronic journals, and study registries.

Journal restrictions vary, but many journals now allow authors to publish supplementary materials with their manuscripts. At minimum, all search strategies, including search strategies for web search engines, websites, conference proceedings databases, electronic journals, and study registries, should be submitted as a supplement for publication. Though most supplements are appropriately accessible on journal publishers’ web sites as submitted, supplements may disappear [ 17 ]. In addition, many supplements are only available to journal subscribers [ 93 ]. Similarly, manuscripts available on public access systems like PubMed Central [ 94 ] may not have the corresponding supplemental materials properly linked. For optimal accessibility, authors should upload complete documentation to a data repository (Table 2 ), an institutional repository, or other secure and permanent online archive instead of relying on journal publication (see Table 3 for additional information).

It is important to document and report the search strategy exactly as run, typically by copying and pasting the search strategy directly as entered into the search platform. This is to ensure that information such as the fields searched, term truncation, and combinations of terms (i.e., Boolean logic or phrases) are accurately recorded. Many times, the copied and pasted version of a search strategy will also include key information such as limits (see Item 9; Table 2 ) used, databases searched within a multi-database search, and other database-specific detail that will enable more accurate reporting and greater reproducibility. This documentation must also repeat the database or resource name, database platform or web address, and other details necessary to clearly describe the resource.

Report the full search strategy in supplementary materials as described above. Describe and link to the location of the supplementary materials in the methods section.

Item 9: Limits and restrictions

Specify that no limits were used, or describe any limits or restrictions applied to a search (e.g., date or time period, language, study design) and provide justification for their use.

No limits . “We imposed no language or other restrictions on any of the searches.” [ 95 ]

Limits described without justification . “The search was limited to the English language and to human studies.” [ 96 ]

“The following search limits were then applied: randomized clinical trials (RCTs) of humans 18 years or older, systematic reviews, and meta-analyses.” [ 97 ]

Limits described with justification . “The search was limited to publications from 2000 to 2018 given that more contemporary studies included patient cohorts that are most reflective of current co-morbidities and patient characteristics as a result of the evolving obesity epidemic.” [ 98 ]

Limits described, one with justification . “Excluded publication types were comments, editorials, patient education handouts, newspaper articles, biographies, autobiographies, and case reports. All languages were included in the search result; non-English results were removed during the review process…. To improve specificity, the updated search was limited to human participants.” [ 99 ]

Many databases have features that allow searchers to quickly restrict a search using limits. What limits are available in a database are unique to both the database and the platform used to search it. Limits are dependent on the accuracy of the indexer, the timeliness of indexing, and the quality of any publisher-supplied data. For instance, using database limits to restrict searches to randomized controlled trials will only find records identified by the indexer as randomized controlled trials. Since the indexing may take 6 months or more to complete for any given article, searchers risk missing new articles when using database limits.

Using database-provided limit features should not be confused with using filters (see Item 10; Table 2 ) or inclusion criteria for the systematic review. For example, systematic review teams may choose to only include English-language randomized controlled trials. This can be done using limits, a combination of a filter (see Item 10) and screening, or screening alone. It should be clear to the reader which approach is used. For instance, in the “ Limits described, with one justification ” example above, the authors used database limits to restrict their search by publication type, but they did not use database limits to restrict by language, even though that was a component of their eligibility criteria. They also used database limits to restrict to human participants in their search update.

It is important for transparency and reproducibility that any database limits applied when running the search are reported accurately, as their use has high potential for introducing bias into a search [ 1 , 64 , 100 , 101 ]. Database limits are not recommended for use in systematic reviews, due to their fallibility [ 39 , 100 ]. If used, review teams should include a statement of justification for each use of a database limit in the methods section, the limitations section, or both [ 102 , 103 ]. In the examples above, only the last two examples provide some justification in the methods section (“to improve specificity” [ 99 ] and “contemporary studies included patient cohorts that are most reflective of current co-morbidities and patient characteristics as a result of the evolving obesity epidemic” [ 98 ]).

Report any limits or restrictions used or that no limits were used in the abstract, methods section, and in any supplementary materials, including the full search strategies (Item 8). Report the justification for any limits used within the methods section and/or in the limitations section.

Item 10. Search filters

Indicate whether published search filters were used (as originally designed or modified), and if so, cite the filter(s) used.

“For our MEDLINE search we added a highly sensitive filter for identifying randomised trials developed by the Cochrane Collaboration [38]. For Embase we used the filter for randomised trials proposed by the Scottish Intercollegiate Guidelines Network [ 104 ].” [ 105 ]

Filters are a predefined combination of search terms developed to identify references with a specific content, such as a particular type of study design (e.g., randomized controlled trials) [ 106 ], populations (e.g., the elderly), or a topic (e.g., heart failure) [ 107 ]. They often consist of a combination of subject headings, free-text terms, and publication types [ 107 ]. For systematic reviews, filters are generally recommended for use instead of limits built into databases, as discussed in Item 9, because they provide the much higher sensitivity (Table 2 ) required for a comprehensive search [ 108 ].

Any filters used as part of the search strategy should be cited, whether published in a journal article or other source. This enables readers to assess the quality of the filter(s) used, as most published search filters are validated and/or peer reviewed [ 106 , 107 ]. Many commonly used filters are published on the InterTASC Information Specialists’ Sub-Group [ 109 ], in the Cochrane Handbook [ 4 , 39 ], and through the Health Information Research Unit of McMaster University [ 110 ].

Cite any search filter used in the methods section and describe adaptations made to any filter. Include the copied and pasted details of any search filter used or adapted for use as part of the full search strategy (Item 8).

Item 11. Prior work

Indicate when search strategies from other literature reviews were adapted or reused for a substantive part or all of the search, citing the previous review(s).

“We included [search strategies] used in other systematic reviews for research design [ 111 ], setting [ 112 , 113 ], physical activity and healthy eating [ 114 , 115 , 116 ], obesity [ 111 ], tobacco use prevention [ 117 ], and alcohol misuse [ 118 ]. We also used a search [strategy] for intervention (implementation strategies) that had been employed in previous Cochrane Reviews [ 119 , 120 ], and which was originally developed based on common terms in implementation and dissemination research.” [ 121 ]

Many authors may also examine previously published search strategies to develop the search strategies for their review. Sometimes, authors adapt or reuse these searches for different systematic reviews [ 122 ]. When basing a new search strategy on a published search strategy, it is appropriate to cite the original publication(s) consulted.

Search strategies differ from filters (Item 10) because search strategies are often developed for a specific project, not necessarily designed to be repeatedly used. Filters, on the other hand, are developed with the express purpose of reuse. Filters are often objectively derived, tested, and validated, whereas most search strategies published as part of systematic review or other evidence synthesis are “best guess,” relying on the expertise of the searcher and review team [ 107 ].

As in the example above, researchers may rely on multiple prior published searches to construct a new search for a novel review. Many times, researchers will use the same searches from a published systematic review to update the existing systematic review. In either case, it is helpful to the readers to understand whether major portions of a search are being adapted or reused.

Report any prior work consulted, adapted, or reused in the methods section. Include the copied and pasted search strategies used, including portions or the entirety of any prior work used or adapted for use, in the full search strategy (Item 8).

Item 12. Updates

Report the methods used to update the search(es) (e.g., rerunning searches, email alerts).

“Ovid Auto Alerts were set up to provide weekly updates of new literature until July 09, 2012.” [ 123 ]

“ Two consecutive searches were conducted and limited by publication type and by date, first from January 1, 1990, to November 30, 2012, and again from December 1, 2012, to July 31, 2015, in an updated search…. The original search strategy was used to model the updated search from December 1, 2012, to July 31, 2015. The updated search strategy was consistent with the original search; however, changes were required in the ERIC database search because of a change in the ERIC search algorithm. Excluded publication types were identical to the initial search. To improve specificity, the updated search was limited to human participants.” [ 99 ]

The literature search is usually conducted at the initial stage of the production of a systematic review. As a consequence, the results of a search may be outdated before the review is published [ 124 , 125 , 126 ]. The last search in a review should be conducted ideally less than 6 months before publication [ 90 , 92 , 125 ]. For this reason, authors often update searches by rerunning (Table 2 ) the same search(es) or otherwise updating searches before the planned publication date. Updating searches differs from updating a systematic review, i.e., when the same or different authors or groups decide to redo a published systematic review to bring its findings up to date. If authors are updating a published systematic review, either authored by the same review team or another, Item 11 contains relevant guidance.

When reporting search updates, the extent of reporting depends on methods used and any changes that were made while updating the searches. If there are no changes in information sources and/or search syntax (Table 2 ), it is sufficient to indicate the date the last search was run in the methods section and in the supplementary materials. If there are any changes in information sources and/or search syntax, the changes should be indicated (e.g., different set of databases, changes in search syntax, date restrictions) in the methods section. Authors should explain why these changes were made. When there were changes in the search strategy syntax, the original and the updated searches should both be reported as described in Item 8.

If authors use email alerts or other methods to update searches, these methods can be briefly described by indicating the method used, the frequency of any updates, the name of the database(s) used, or other relevant information that will help readers understand how the authors conducted search updates. If deduplication methods are used as part of the search update process, these methods can be described using guidance in Item 16.

Report the methods used to update the searches in the methods section and the supplementary materials, as described above.

Item 13. Dates of searches

For each search strategy, provide the date when the last search occurred.

“A comprehensive literature search was initially run on 26 February 2017 and then rerun on 5 February 2018….” [ 127 ]

Most literature databases are regularly updated with new citations as articles are published. Citations already in the database may also be updated once new information (such as indexing terms or citing articles) is available. As an example, MEDLINE added over 900,000 indexed citations (Table 2 ) in fiscal year 2018 [ 41 ]. In addition, the information gathered by databases (such as author affiliations in MEDLINE) can change over time. Because new citations are regularly being added, systematic review guidelines recommend updating searches throughout the writing process to ensure that all relevant articles are retrieved [ 6 , 92 ].

It is necessary for authors to document the date when searches were executed, either the date the initial search was conducted, if only searched once, or the most recent date the search was rerun. This allows readers to evaluate the currency of each search and understand what literature the search could have potentially identified [ 125 ]. In addition, it supports reproducibility and updating by allowing other researchers to use date limits to view the same “slice” of the database that the original authors used or to update a systematic review by searching from the last time point searched.

Report the date of the last search of the primary information sources used in the abstract for optimal clarity for readers [ 128 ]. Report the time frame during which searches were conducted, the initial search date(s), and/or the last update search date(s) in the methods section. Report the initial and/or last update search date with each complete search strategy in the supplementary materials, as in the examples for Item 8.

Item 14. Peer review

Describe any search peer review process.

“The strategies were peer reviewed by another senior information specialist prior to execution using the PRESS Checklist [ 1 ].” [ 129 ]

Peer reviewing search strategies is an increasingly valued component of search strategy development for systematic reviews. Expert guidance recommends taking this step to help increase the robustness of the search strategy [ 6 , 74 ]. Peer reviewing (Table 2 ) searches is useful to help to guide and improve electronic search strategies. One of peer review’s main benefits is the reduction of errors [ 23 , 130 ]. Peer review may also increase the number of relevant records found for inclusion in reviews, thus improving the overall quality of the systematic review [ 131 ].

Authors should consider using the Peer Review of Electronic Search Strategies (PRESS) Guideline statement, a practice guideline for literature search peer review outlining the major components important to review and the benefits of peer reviewing searches [ 1 ]. Authors should strongly consider having the search strategy peer reviewed by an experienced searcher, information specialist, or librarian [ 1 , 131 ]. Though peer review may be conducted generally with publication of a protocol, for example, this item is designed to document search-specific peer review.

Describe the use of peer review in the methods section.

Item 15. Total records

Document the total number of records identified from each database and other information sources.

Methods section . “A total of 3251 citations were retrieved from the six databases and four grey literature websites.” [ 133 ] Flow diagram . Fig. 1 . Fig. 1 “Figure 1. PRISMA 2009 flow diagram” [ 132 ] Full size image

Recording the flow of citations through the systematic review process is a key component of the PRISMA Statement [ 9 , 35 ]. It is helpful to identify how many records (Table 2 ) were identified within each database and additional source. Readers can use this information to see whether databases or expert contacts constituted the majority of the records reviewed, for example. Knowing the number of records from each source also helps with reproducibility. If a reader tries to duplicate a search from a systematic review, one would expect to retrieve nearly the same results when limiting to the timeframe in the original review. If instead, the searcher locates a drastically different number of results than reported in the original review, this can be indicative of errors in the published search [ 23 ] or major changes to a database, both of which might be reasons to update a systematic review or view the systematic review’s results with skepticism.

Report the total number of references retrieved from all sources, including updates, in the results section. Report the total number of references from each database and information source in the supplementary materials. If space permits, report the total number of references from each database in the PRISMA flow diagram [ 35 ].

Item 16. Deduplication

Describe the processes and any software used to deduplicate records from multiple database searches and other information sources.

“Duplicates were removed by the librarians (LP, PJE), using EndNote's duplicate identification strategy and then manually.” [ 134 ]

Databases contain significant overlap in content. When searching in multiple databases and additional information sources, as is necessary for a systematic review, authors often employ a variety of techniques to reduce the number of duplicates within their results prior to screening [ 135 , 136 , 137 , 138 ]. Techniques vary in their efficacy, sensitivity, and specificity (Table 2 ) [ 136 , 138 ]. Knowing which method is used enables readers to evaluate the process and understand to what extent these techniques may have removed false positive duplicates [ 138 ]. Authors should describe and cite any software or technique used, when applicable. If duplicates were removed manually, authors should include a description.

Report any deduplication method used in the methods section. The total number of references after deduplication should be reported in the PRISMA flow diagram [ 35 ].

Part 5. Discussion and conclusions

The PRISMA-S extension is designed to be used in conjunction with PRISMA 2020 [ 35 ] and PRISMA extensions including PRISMA-P for protocols [ 36 ], PRISMA-ScR for scoping reviews [ 139 ], the PRISMA Network Meta-analyses statement [ 140 ], and PRISMA-IPD for systematic reviews using individual patient data [ 141 ]. It may also be used with other reporting guidelines that relate to systematic reviews and related review types, such as RepOrting standards for Systematic Evidence Syntheses (ROSES) [ 142 ]. It provides additional guidance for systematic review teams, information specialists, librarians, and other researchers whose work contains a literature search as a component of the research methods. Though its origins are in the biomedical fields, PRISMA-S is flexible enough to be applied in all disciplines that use method-driven literature searching. Ultimately, PRISMA-S attempts to give systematic review teams a framework that helps ensure transparency and maximum reproducibility of the search component of their review.

PRISMA-S is intended to capture and provide specific guidance for reporting the most common methods used in systematic reviews today. As new methods and information sources are adopted, authors may need to adjust their reporting methods to accommodate new processes. Currently, PRISMA-S does not address using text mining or text analysis methods to create the search, for example, though this is an increasingly common way for information specialists to develop robust and objective search strategies [ 143 , 144 , 145 ]. Likewise, PRISMA-S does not require that decisions about the rationale behind choices in search terms and search construction be recorded, though this provides readers a great deal of insight. In the future, methods and rationales used to create search strategies may become more important for reproducibility.

PRISMA-S offers extensive guidance for many different types of information source and methods, many of them not described in detail in other reporting guidelines relating to literature searching. This includes detailed information on reporting study registry searches, web searches, multi-database searches, and updates. PRISMA-S can help authors report all components of their search, hopefully making the reporting process easier. As a note, PRISMA-S provides guidance on transparent reporting to authors and is not intended as a tool to either guide conduct of a systematic review or to evaluate the quality of a search or a systematic review.

The PRISMA-S checklist is available for download in Word and PDF formats from the PRISMA Statement web site [ 37 ]. The checklist should be used together with its Explanation & Elaboration documentation to provide authors with guidance for the complexities of different types of information sources and methods.

We intend to work with systematic review and information specialist organizations to broadly disseminate PRISMA-S and encourage its adoption by journals. In addition, we plan to host a series of webinars discussing how to use PRISMA-S most effectively. These webinars will also be available for later viewing and will serve as a community resource.

We hope that journal editors will recommend authors of systematic reviews and other related reviews to use PRISMA-S and submit a PRISMA-S checklist with their manuscripts. We also hope that journal editors will encourage more stringent peer review of systematic review searches to ensure greater transparency and reproducibility within the review literature.

Availability of data and materials

All data is available via the PRISMA-S PRISMA Search Reporting Extension OSF site ( https://doi.org/10.17605/OSF.IO/YGN9W ) [ 32 ]. This includes all data relating to item development, survey instruments, data from the Delphi surveys, and consent documents.

Abbreviations

Digital object identifier

Peer Review of Electronic Search Strategies

Preferred Reporting Items for Systematic reviews and Meta-Analyses

PRISMA for individual patient data

PRISMA for systematic review protocols

PRISMA for scoping reviews

RepOrting standards for Systematic Evidence Syntheses

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Acknowledgements

We would like to thank all of the members of the PRISMA-S Group, which is comprised of participants in the Delphi process, consensus conference, or both. PRISMA-S Group members include Heather Blunt (Dartmouth College), Tara Brigham (Mayo Clinic in Florida), Steven Chang (La Trobe University), Justin Clark (Bond University), Aislinn Conway (BORN Ontario and CHEO Research Institute), Rachel Couban (McMaster University), Shelley de Kock (Kleijnen Systematic Reviews Ltd), Kelly Farrah (Canadian Agency for Drugs and Technologies in Health (CADTH)), Paul Fehrmann (Kent State University), Margaret Foster (Texas A & M University), Susan A. Fowler (Washington University in St. Louis), Julie Glanville (University of York), Elizabeth Harris (La Trobe University), Lilian Hoffecker (University of Colorado Denver), Jaana Isojarvi (Tampere University), David Kaunelis (Canadian Agency for Drugs and Technologies in Health (CADTH)), Hans Ket (VU Amsterdam), Paul Levay (National Institute for Health and Care Excellence (NICE)), Jennifer Lyon, Jessie McGowan (uOttawa), M. Hassan Murad (Mayo Clinic), Joey Nicholson (NYU Langone Health), Virginia Pannabecker (Virginia Tech), Robin Paynter (VA Portland Health Care System), Rachel Pinotti (Icahn School of Medicine at Mount Sinai), Amanda Ross-White (Queens University), Margaret Sampson (CHEO), Tracy Shields (Naval Medical Center Portsmouth), Adrienne Stevens (Ottawa Hospital Research Institute), Anthea Sutton (University of Sheffield), Elizabeth Weinfurter (University of Minnesota), Kath Wright (University of York), and Sarah Young (Carnegie Mellon University). We would also like to thank Kate Nyhan (Yale University), Katharina Gronostay (IQWiG), the many others who contributed to the PRISMA-S project anonymously or as draft reviewers, and our peer reviewers. We would like to give special thanks to the late Douglas G. Altman (D.G.A.; University of Oxford) for his support and guidance, and the co-chairs of the Medical Library Association’s Systematic Reviews SIG in 2016, Margaret Foster (Texas A & M University) and Susan Fowler (Washington University in St. Louis), for allowing us to use one of their meeting times for the consensus conference.

Melissa Rethlefsen was funded in part by the University of Utah’s Center for Clinical and Translational Science under the National Center for Advancing Translational Sciences of the National Institutes of Health Award Number UL1TR002538 in 2017–2018 . The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

Shona Kirtley was funded by the Cancer Research UK (grant C49297/A27294). The funder had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript. The views expressed are those of the authors and not necessarily those of the Cancer Research UK.

Matthew Page is supported by an Australian Research Council Discovery Early Career Researcher Award (DE200101618).

David Moher is supported by a University Research Chair, University of Ottawa, Ottawa, Canada.

The consensus conference was sponsored by the Systematic Reviews SIG of the Medical Library Association. There was no specific funding associated with this event.

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Heather Blunt
, Tara Brigham
, Steven Chang
, Justin Clark
, Aislinn Conway
, Rachel Couban
, Shelley de Kock
, Kelly Farrah
, Paul Fehrmann
, Margaret Foster
, Susan A. Fowler
, Julie Glanville
, Elizabeth Harris
, Lilian Hoffecker
, Jaana Isojarvi
, David Kaunelis
, Paul Levay
, Jennifer Lyon
, Jessie McGowan
, M. Hassan Murad
, Joey Nicholson
, Virginia Pannabecker
, Robin Paynter
, Rachel Pinotti
, Amanda Ross-White
, Margaret Sampson
, Tracy Shields
, Adrienne Stevens
, Anthea Sutton
, Elizabeth Weinfurter
, Kath Wright
& Sarah Young

Contributions

M.L.R. conceived and designed the study, conducted the thematic and quantitative analyses, curated the data, drafted the manuscript, and reviewed and edited the manuscript. M.L.R. is the guarantor. J.B.K. and S.K. contributed to the design of the study, developed the literature search strategies, contributed to the thematic content analyses, drafted a portion of the Elaboration & Explanation, and reviewed and edited the manuscript. J.B.K. developed the survey instrument. M.L.R., J.B.K., and S.K. hosted and organized the consensus conference. S.W. and A.P.A. contributed to the thematic content analysis, drafted a portion of the Elaboration & Explanation, and reviewed and edited the manuscript. S.W. supervised the draft revision documentation. D.M. helped conceive and design the study. M.J.P. provided substantive review and editing of the checklist, Explanation & Elaboration, and final manuscript. The author (s) read and approved the final manuscript.

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Correspondence to Melissa L. Rethlefsen .

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This study was declared exempt by the University of Utah Institutional Review Board (IRB_00088425). Consent was received from all survey participants.

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The authors declare no competing interests. MJP and DM are leading the PRISMA 2020 update.

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Rethlefsen, M.L., Kirtley, S., Waffenschmidt, S. et al. PRISMA-S: an extension to the PRISMA Statement for Reporting Literature Searches in Systematic Reviews. Syst Rev 10 , 39 (2021). https://doi.org/10.1186/s13643-020-01542-z

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Received : 28 February 2020

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Published : 26 January 2021

DOI : https://doi.org/10.1186/s13643-020-01542-z

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Turk Arch Otorhinolaryngol
v.57(1); 2019 Mar

A Guide for Systematic Reviews: PRISMA

Dear Editor,

In Turkish Otorhinolaryngology publications reviews are often written in the form of an account, and systematic reviews and meta analyses are rarely performed ( 1 – 4 ). A systematic approach to a review, however, will minimize bias and maximize its contribution to science. Including meta-analysis in a review will carry the publication to the highest level of evidence. This will also significantly increase the citability of the report.

As the Turkish Archives of Otorhinolaryngology is the scientific open access journal of our society, this scientific letter aims to reach our colleagues who plan on writing reviews in the field of otorhinolaryngology with the use of PRISMA guidelines for the purpose of standardizing systematic review writing.

According to the common opinion, a review type article is the interpretation, synthesis and assessment of the scientific reports and studies printed in scientific publications by authors experienced in the area ( 5 ). Reviews written with an analogous approach cannot go beyond an account of what has been already done: They cover a wide range of topics within a given subject; may be useful in understanding new concepts, but are rarely comprehensive; rarely give details about the methods; are likely to be written in line with the opinions of the author; quality differences between the studies are rarely considered; and as a result, can be misinterpreted and lead to inadvertent bias.

To avoid these issues in systematic review writing, the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) group, which mainly consists of Cochrane authors, has developed the PRISMA guidelines in 2009 ( 6 ). A systematic review will extensively scan all reports published on the subject to find the answers to a clearly defined research question, and to that end will use various inclusion and exclusion criteria to identify the reports to be included in the review, and then synthesize the findings. Using statistical methods for the interpretation of the results implies a systematic review containing meta-analysis ( 6 ).

The PRISMA guidelines consist of a four-phase flow diagram and a 27-item checklist. The flow diagram describes the identification, screening, eligibility and inclusion criteria of the reports that fall under the scope of a review. The checklist includes a 27-item recommendation list on topics such as title, abstract, introduction, methods, results, discussion and financing. With this flow diagram and checklist, PRISMA items serve as a guide for authors, reviewers and editors.

PRISMA extensions can be reached at their website: www.prisma-statement.org ( 7 ). The Turkish translations of the flow diagram and the checklist can also be found here. The website also includes a scientific report authored by the PRISMA group that gives examples to a systematic review in line with the guidelines, as well as detailed explanations and descriptions ( 8 ). All content related to the PRISMA guidelines are open access for the purposes of disseminating its utilization.

Full compliance with the checklist items will facilitate clarity and transparency in reporting; and thereby enable a structured report that well-defines the study question, clearly states its title and objectives, benefits from a comprehensive strategy for identifying all relevant study reports, clearly and justifiably indicates inclusion and exclusion criteria, critically and accurately prioritizes the reviewed study reports, provides a clear analysis of the eligible study reports based on qualitative and—where applicable in relation to the data—quantitative (meta-analysis) content.

As stated in the ‘Instructions for Authors’ page of your journal, the PRISMA items are the recommended reporting method to be adopted in order to avoid the basic mistakes in systematic review and meta-analysis reports. I believe that wider adoption of these guidelines in our country will significantly contribute to the otorhinolaryngology reports published in Turkey.

Acknowledgements

I would like to thank Prof. Cenk Ecevit, MD for raising my awareness on this issue, hence causing me to write this scientific letter.

This study was presented at the A to Z Scientific Study Planning, Writing and Publishing Processes Meeting in Health Sciences, January 9 2019, Sivas, Turkey.

Peer-review: Externally peer-reviewed.

Conflict of Interest: The author has no conflicts of interest to declare.

Financial Disclosure: The author declared that this study has received no financial support.

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Rethlefsen, M. L., Kirtley, S., Waffenschmidt, S., Ayala, A. P., Moher, D., Page, M. J., Koffel, J. B., & PRISMA-S Group (2021). PRISMA-S: an extension to the PRISMA Statement for Reporting Literature Searches in Systematic Reviews. Systematic reviews, 10(1), 39. https://doi.org/10.1186/s13643-020-01542-z
Shamseer L, Moher D, Clarke M, Ghersi D, Liberati A, Petticrew M, Shekelle P, Stewart LA, the PRISMA-P Group. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: elaboration and explanation. BMJ 2015;349:g7647. https://doi.org/10.1136/bmj.g7647
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Peer-reviewed

Research Article

Epidemiology of human and animal leptospirosis in Kenya: A systematic review and meta-analysis of disease occurrence, serogroup diversity and risk factors

Roles Conceptualization, Formal analysis, Funding acquisition, Investigation, Methodology, Project administration, Resources, Supervision, Validation, Visualization, Writing – original draft, Writing – review & editing

* E-mail: [email protected] (MW); [email protected] (EAJC)

Affiliation Department of Biological Safety, German Federal Institute for Risk Assessment, Berlin, Germany

Roles Methodology, Validation, Writing – review & editing

Affiliation Animal and Human Health Department, International Livestock Research Institute, Nairobi, Kenya

Roles Methodology, Resources, Supervision, Writing – review & editing

Martin Wainaina,
Joseph Wasonga,
Elizabeth Anne Jessie Cook

Published: September 27, 2024
https://doi.org/10.1371/journal.pntd.0012527
Reader Comments

This is an uncorrected proof.

Leptospirosis is a priority zoonotic disease in Kenya, but an in-depth review of its presence in humans, animals and the environment is lacking. Therefore, we conducted this systematic review and meta-analysis to understand the epidemiological situation to date.

Methodology

We searched for literature in African journals online, AGRIS, Embase, the Leptospira WOAH reference laboratory library, ProMED-mail, PubMed, Scopus, Web of Science, and the institutional repositories of 33 academic institutions and included 66 publications on leptospirosis in Kenya which spanned from 1951 to 2022. The review was registered on the International Platform of Registered Systematic Review and Meta-analysis Protocols (INPLASY).

Most investigations were done in rural and urban areas in western, southern, central, and coastal areas in Kenya and the largely pastoral eastern and northern areas were under-represented. A wide host range of domestic animals and wildlife was revealed, and occupational exposure was an important risk factor for humans. The microscopic agglutination test (MAT) was the most frequent test, particularly common in studies conducted during the 1980s and 1990s. However, varying MAT panels and cut-off titres were observed. The overall seroprevalence in cattle was 28.2% (95% confidence intervals [CI]: 12.0–53.0; heterogeneity: I 2 = 96.7%, τ 2 = 1.4), and 11.0% in goats (95% CI: 5.4–21.2; heterogeneity: I 2 = 78.8%, τ 2 = 0.4). Molecular tests were seldom used to determine species and illustrate strain diversity. There was a lack of awareness of leptospirosis among farmers and health practitioners.

The widespread presence of leptospires and inadequate diagnostic capacity demonstrate that leptospirosis is a common but underreported disease in Kenya. Raising awareness and boosting the country’s diagnostic capacity is crucial to timely detection and disease control.

Author summary

Leptospirosis is a prevalent but understudied zoonotic disease in Kenya. A comprehensive review of the presence of the disease in various hosts is therefore needed to catalogue the research efforts and inspire future scientific inquiry on this neglected tropical disease. We therefore undertook this comprehensive review of published literature in leading databases and institutional repositories of relevant Kenyan higher institutions of learning. Literature spanning more than 70 years was identified and study areas showed a regional bias towards central, western, southern and coastal regions. The arid and semi-arid areas in the northern and eastern regions with large animal and wildlife populations that could facilitate leptospiral transmission were under-represented, and the inclusion of these pastoral regions could give a better picture of the country’s leptospirosis risk profile. Summary estimates in cattle and goats revealed considerable pooled seroprevalence of leptospirosis and the need for control in animal hosts. A low awareness among farmers, and animal and public health practitioners was found, demonstrating the need for education initiatives that can facilitate at-risk populations such as farmers. Additionally, the country lacks the capacity for MAT testing, and recent efforts to culture for leptospires are non-existent. Understanding the circulating serovars and strain diversity is crucial to the effective control of leptospirosis. Investments in diagnostics for peripheral and central laboratories are vital for public health response.

Citation: Wainaina M, Wasonga J, Cook EAJ (2024) Epidemiology of human and animal leptospirosis in Kenya: A systematic review and meta-analysis of disease occurrence, serogroup diversity and risk factors. PLoS Negl Trop Dis 18(9): e0012527. https://doi.org/10.1371/journal.pntd.0012527

Editor: Claudia Munoz-Zanzi, University of Minnesota, UNITED STATES OF AMERICA

Received: April 16, 2024; Accepted: September 10, 2024; Published: September 27, 2024

Copyright: © 2024 Wainaina et al. This is an open access article distributed under the terms of the Creative Commons Attribution License , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Data Availability: All data relating to the present study are available in this manuscript and supplementary files .

Funding: This work was supported by the German Federal Institute for Risk Assessment (BfR) and the CGIAR Initiative on One Health (CGL003: https://www.cgiar.org/initiative/one-health/ ). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.

Competing interests: The authors have declared that no competing interests exist.

Introduction

Leptospirosis is a common but neglected zoonotic disease in the world [ 1 ]. It is caused by bacteria of the genus Leptospira which are finely coiled, obligate aerobic, Gram-negative, catalase-producing, flagellated spirochetes [ 2 ]. The genus includes more than 250 serovars and species are currently classified based on whole genome sequencing (WGS) into the P clade and S clade which consist of subclades P1 (formerly pathogenic), P2 (formerly intermediates), S1 (formerly saprophytes) and S2 (a new subclade) [ 3 ].

Leptospira can infect a wide range of mammalian hosts which can act as reservoirs of the bacteria, but rodents are the most important. Humans primarily acquire leptospirosis either directly via contact with an infected animal or indirectly when in contact with soil or water contaminated with urine from an infected animal [ 4 ]. After infection, the bacteria colonise the renal tubules where they multiply and are eventually shed in urine. Exposure to the bacteria can happen occupationally (e.g., slaughterhouse work), recreationally (e.g., through water sports) or after extreme weather events such as heavy rainfall and flooding [ 4 ]. Areas with inadequate housing and poor sanitation such as informal settlements have an increased risk of exposure [ 4 ]. Human-to-human transmission is rare [ 5 ].

Human leptospirosis can initially present as an acute febrile illness which may resolve after a short period. Some patients can present with the severe late-phase stages of the disease which tend to be fulminant, Weil’s disease and leptospirosis-associated pulmonary haemorrhage syndrome being examples having high case fatality rates [ 6 ]. Animal leptospirosis is characterised by decreased productivity and reproductive losses such as abortions and stillbirths [ 7 ]. Leptospires tend to exhibit host-specificity due to the evolution of their virulence genes to adapt to their preferred hosts [ 8 , 9 ]. An example of this is the Malagasy Leptospira which show specificity towards tenrecs and other small mammals of Madagascar [ 10 ].

Leptospirosis is an important cause of febrile illnesses in Africa [ 11 ] and a zoonotic disease prioritised for control in Kenya [ 12 ]. A recent outbreak of leptospirosis in Tanzania that affected 20 people and caused three fatalities indicates that the disease may be re-emerging in the region [ 13 ]. An in-depth review of the range of hosts, risk factors, diagnostic methods used, prevalent leptospiral serovars and prevalence estimates in various hosts will improve knowledge of this neglected zoonosis in the country. This is critical in control and prevention strategies. Therefore, we conducted this systematic review of leptospirosis in humans and animals in Kenya to answer these questions, reveal key knowledge gaps to inspire future research and inform control strategies.

Literature search

We searched for literature according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [ 14 ] in African journals online, the AGRIS (FAO) database, Embase, ProMED-mail, PubMed, Scopus, Web of Science, and the institutional repositories of 33 Kenyan universities and colleges. The review was registered on the International Platform of Registered Systematic Review and Meta-analysis Protocols (INPLASY) under registration number INPLASY202470097. We used the search terms “leptospirosis”, “leptospira”, “leptospir*”, “Weil disease”, “Weil’s disease”, “Weils disease”, “Spirochaetal jaundice”, “human”, “wildlife”, “domestic”, “rodent”, “ruminant”, “cattle/bovine”, “camel/dromedary”, “sheep/ovine”, “goat/caprine”, “prevalence”, “incidence”, “prevention”, “control”, “risk” and “Kenya”. The search terms were combined using different Boolean operators and the terms were modified to fit the needs of the various databases as presented in S1 Data . We set no time limit and allowed all languages. The searches were conducted on 14 February 2023. Lastly, we checked for relevant literature on isolates originating from Kenya on the website of the World Organisation for Animal Health (WOAH) reference laboratory for leptospirosis [ 15 ].

Inclusion and exclusion criteria

We imported references and their abstracts into EndNote software 21 (Thomson Reuters, Philadelphia, PA, USA) and removed duplicate records. We screened the remaining records by title and abstract for eligibility. Studies based on animal and human populations in/originally from Kenya investigating any aspect (both qualitative and quantitative research) of leptospirosis were retained. We excluded records not focussed on leptospirosis, those investigating non-Kenyan populations, and those focussing on travellers. We allowed burden of disease estimations, case reports, case series, cohort, cross-sectional, diagnostic evaluations, outbreak investigations, post-mortem investigations, qualitative studies and study proposals. Grey literature was also permitted (conference proceedings, abstracts, reports and theses). We excluded books and book sections and scanned the reference sections of relevant reviews for articles not captured in our database searches.

Data extraction

Two authors (MW and JW) screened the articles for inclusion and extracted the data and disagreements on the inclusion criteria were settled in consultation with the third author (EAJC). The DeepL translation tool was used for non-English and non-German literature [ 16 ]. Data on the study location, study hosts (animal/human/both), study type, study period, human population settings (community or hospital), animal species, diagnostic test applied, samples tested, number tested and number positive, leptospiral species/serovars/serogroups identified, culture and/or PCR technique, and risk factors for exposure were extracted when available. Clinical signs and symptoms in humans were also obtained from leptospirosis cases confirmed by culture or antibody titre rise.

Statistical analysis

The data were imported into R version 4.3.2 where summary statistics were computed and plots and maps were generated to represent the spatial and temporal distribution of publications. Additionally, the microscopic agglutination test (MAT) panel diversity was plotted and the serogroups identified in various hosts by culture and serological methods were illustrated using an alluvial diagram made by the ggalluvial package [ 17 ]. Lastly, the hosts were categorised into three epidemiological compartments (human, domestic animals and wildlife) and the serogroups determined by MAT titres ≥1:100 (presence/absence data) were used to calculate the serogroup diversity (richness and evenness) by computing the Shannon, Simpsons, and Inverse Simpson indexes using the vegan package [ 18 ]. The Kruskal-Wallis test was applied to each of the three diversity indexes to assess statistically significant differences across the three compartments.

Meta-analysis

Due to the paucity of data and diverse diagnostic methods and cut-offs utilised to determine positive cases, we did not estimate the summary effects in sheep and humans (considering community and hospital subpopulations). However, cross-sectional studies published in peer-reviewed journal articles that reported the prevalence in cattle and goats as tested from blood, serum or kidney samples using all diagnostic tests (MAT titres ≥1:100) were utilised in the meta-analysis to minimise the risk of bias. A random effects model was fitted on untransformed proportions. The metaprop command in the meta package [ 19 ] was used to pool studies using the logit transformed proportions (PLO) option. Study heterogeneity (Tau square or τ 2 ) was estimated using the restricted maximum likelihood (REML) method and a Hartung-Knapp adjustment was applied. Higgins’ I 2 statistic that quantifies study heterogeneity was reported as well. The results were visualised on forest plots with the diagnostic tests utilised as sub-groups and studies were arranged according to the publication year to illustrate any trends in prevalence with time.

We initially identified 1,435 records from our database search and 66 were finally included in the qualitative and quantitative analyses. A summary of the study selection process is presented in Fig 1 . Articles that were finally included were in English, Dutch or German.

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https://doi.org/10.1371/journal.pntd.0012527.g001

The included publications were widely distributed across Kenya ( Fig 2 ), spanning from 1951 to 2022. There was an initial increase in the publication numbers until the 1970s, followed by a subsequent decline until 2010 when a sharp spike in the publication numbers was observed. Additionally, most studies focused on the central, coastal, southern and western regions of the country, and the expansive arid and semi-arid lands in the eastern and northern regions received less attention.

a Study sites of the included records investigating leptospires in Kenya presented by study types for various hosts. b Various article types investigating leptospires from 1951 to 2022 (geoBoundaries, https://www.geoboundaries.org/countryDownloads.html ).

https://doi.org/10.1371/journal.pntd.0012527.g002

Study characteristics

Journal articles were common (n = 49), and a few theses (n = 9), outbreak alerts on ProMED mail (n = 5) and abstracts (n = 3) were found. Cross-sectional studies formed the majority of the included publications (n = 37). Other types of reports included outbreak alerts and investigations (n = 11), diagnostic test evaluations (n = 4), isolate characterisations (n = 4), investigations on the knowledge attitudes and practices (KAP) [n = 3], post-mortem characterisations of leptospirosis cases [pathology studies] (n = 2), longitudinal/prospective cohort (n = 1), the protocol of a proposed study [study protocol] (n = 1), and estimation of the burden of disease in Kenya via disability-adjusted life years (DALY) and incidence rates (n = 2). Studies investigating humans (n = 33) and domestic animals (n = 22) were several and a few investigated wildlife (n = 6), both humans and domestic animals (n = 2), humans, domestic animals and wildlife (n = 1), and domestic animals and wildlife (n = 1).

Of the studies that involved humans (n = 37), the majority examined participants in community settings (n = 17) and outpatients in hospital settings (n = 15), and a few recruited both hospital and community participants (n = 5). A summary of the characteristics of studies on animals and human hosts is presented in S1 Table .

Diagnostic methods

Serological testing was the most prominently found diagnostic method used in the study, applied in 34 studies. The serological gold standard diagnostic test, MAT, was the most commonly utilised to determine serovars (18/30). MAT panels used varied in composition and set different cut-offs of 1:30, 1:40, 1:50, 1:100, 1:200, and 1:3000 ( S1 Table ). Notably, two of these studies were from the 1960s, three from the 1970s, five from the 1980s, five from the 1990s, one from the 2000s and the remaining two from 2019 and 2022 ( Fig 3 ).

a Flow diagram illustrating the distribution of serogroups identified by culture and serological methods in various hosts in the country. Each stream presented in a unique colour and width represents the interconnectedness and number of cases in each category. b A distribution of the diagnostic tests applied to determine and characterise leptospires in the included studies over time. c Bar plot showing the count of serogroups represented in microscopic agglutination test (MAT) panels from included studies.

https://doi.org/10.1371/journal.pntd.0012527.g003

Commercially available ELISA tests were used in a few studies (n = 8) [ 20 – 27 ] which all collectively identified serogroups Australis, Canicola, Celledoni, Djasiman, Grippotyphosa, Hebdomadis, Icterohaemorrhagiae, Mini, Pomona, Sejroe, and Tarassovi.

Eleven studies investigated leptospires using molecular tests, targeting the ribosomal 16S rRNA gene ( rrs ) via direct PCR [ 28 – 30 ] and amplicon sequencing [ 31 ], lipL32 [ 32 – 34 ], secY [ 24 , 35 , 36 ], and flab [ 33 ] genes. One study (conference abstract) lacked information on the PCR target [ 37 ]. All studies utilising PCR were conducted between the years 2011 and 2022 ( Fig 3 ).

Culture was used in seven studies to cultivate leptospires from whole blood and kidney tissues using Cox’s [ 38 ], Ellinghausen–McCullough–Johnson–Harris (EMJH) [ 39 ], Fletcher’s [ 38 , 40 – 42 ] and Korthof’s media [ 40 , 43 , 44 ] with animal inoculation being used in some studies [ 38 , 40 , 43 , 44 ]. We found no recent studies utilising culture, with the last one being published in 1987 ( Fig 3 ). Lastly, the first descriptions of the serovars (reference strain, serogroup) kanana (Kanana, Tarassovi) [ 45 ], lambwe (Lambwe, Autumnalis) [ 45 ], kenya (Njenga, Ballum) [ 45 ], kwale (Julu, Pyrogenes) [ 46 ], ramisi (Musa, Australis) [ 47 ], and nyanza (Kibos, Hebdomadis) [ 48 ] were found as determined by the cross-agglutination absorption test (CAAT).

Prevalence distribution

Several studies surveyed leptospires using serological and molecular tests in domestic animals which included cattle (n = 16) [ 21 – 23 , 36 , 38 , 39 , 43 , 44 , 49 – 56 ], goats (n = 11) [ 34 , 36 , 38 , 43 , 51 , 52 , 55 , 57 – 60 ], sheep (n = 8) [ 34 , 38 , 43 , 51 , 52 , 55 , 56 , 58 ], dogs (n = 2) [ 38 , 54 ], pigs (n = 2) [ 36 , 61 ], donkeys (n = 1) [ 38 ], chicken (n = 1) [ 36 ], fish (n = 1) [ 36 ], and camels (n = 1) [ 36 ]. Seropositivity estimates varied widely in cattle (range: 0.8% to 85.9%), sheep (0.0% to 26.1%) and goats (2.6% to 46.9%). A summary of the study characteristics is presented in S1 Table . One study estimated the incidence of leptospirosis in both seroconverted sheep and goats to be 1.8 cases per 100 animal-months at risk each [ 34 ]. The meta-analysis performed on results from journal articles revealed an overall seroprevalence of bovine leptospirosis of 28.6% (95% confidence intervals [CI]: 4.7–76.5) by the MAT test and 26.6% (95% CI: 12.8–47.1) by ELISA. The overall seroprevalence in 3,311 cattle included was 28.2% (95% CI: 12.0–53.0), and high between-study heterogeneity was found ( I 2 = 96.7%, τ 2 = 1.4) ( Fig 4 ). Similarly, the pooled seroprevalence of caprine leptospirosis by MAT that included 1,850 goats was 11.0% (95% CI: 5.4–21.2), with a high between-study heterogeneity being observed ( I 2 = 78.8%, τ 2 = 0.4) ( Fig 4 ).

https://doi.org/10.1371/journal.pntd.0012527.g004

Wildlife were investigated with a specific focus on rodents and small mammals (n = 4) [ 24 , 31 , 35 , 38 ], gazelles (n = 2) [ 60 , 62 ], elands (n = 2) [ 60 , 62 ], giraffes (n = 2) [ 60 , 62 ], topis (n = 2) [ 54 , 60 ], rhinos (n = 2) [ 54 , 63 ], wildebeests (n = 1) [ 39 ], hartebeests (kongonis, n = 1) [ 64 ], dik-diks (n = 1) [ 64 ], bongos (n = 1) [ 64 ], cheetahs (n = 1) [ 57 ], lions (n = 1) [ 62 ], waterbucks (n = 1) [ 64 ], zebras (n = 1) [ 58 ], hippopotamuses (n = 1) [ 58 ], sunis (n = 1) [ 58 ], buffaloes (n = 1) [ 39 ], elephants (n = 1) [ 62 ], and impala (n = 1) [ 64 ]. A summary of seropositive animals and other study characteristics is given in S1 Table .

Several studies on human populations were found in healthcare [ 25 , 27 , 28 , 30 , 33 , 37 , 41 , 42 , 65 ] and community [ 20 , 26 , 32 , 38 , 52 , 65 ] settings. Seropositivity estimates in community populations ranged from 2.5% to 25.7% and those in hospitals from 0.5% to 25.0% ( S1 Table ). Estimates of the burden of disease in Kenya from the Leptospirosis Epidemiology Reference Group (LERG) of the World Health Organisation (WHO) revealed the disease is responsible for a mean estimate of 67,596 DALYs annually in the country [ 66 ]. The LERG group also estimated an annual incidence of human leptospirosis of 2.9 cases per 100,000 population in the country [ 67 ].

Serovar and species distribution

The MAT panel used in studies varied substantially ( Fig 3 ). The five most frequently investigated serogroups were Icterohaemorrhagiae (n = 28), Sejroe (n = 26), Grippotyphosa (n = 22), Canicola (n = 20), and Australis (n = 19). The least comprised Mini (n = 5), Panama (n = 2), Shermani (n = 2), Djasiman (n = 1) and Manhao (n = 1). When the diversity of serogroups observed via serology in hosts categorised into human, wildlife and domestic animal compartments was determined, a greater serogroup diversity was observed in domestic animals using all diversity indexes applied (Shannon = 2.77, Simpson = 0.94, Inverse Simpson = 16). The human compartment showed less diversity (Shannon = 2.56, Simpson = 0.92, Inverse Simpson = 13) and wildlife species showed the least serogroup diversity (Shannon = 2.2, Simpson = 0.89, Inverse Simpson = 9) ( Fig 5 ). The three separate Kruskal-Wallis tests conducted to assess the serogroup diversity estimates in the three compartments for each of the three indexes (Shannon, Simpson, and Inverse Simpson) all returned identical results, with a p-value of 0.37.

The diversity indexes demonstrate serogroup richness and evenness. Kruskal-Wallis test results showed no statistically significant differences in the serogroup diversity across the domestic, wildlife and human hosts using all three indexes (p-values = 0.37).

https://doi.org/10.1371/journal.pntd.0012527.g005

Three studies used molecular tools to identify genomospecies, with single locus sequence typing (SLST) based on the secY gene, showing L . interrogans [ 24 , 35 , 36 ] and L . kirschneri [ 35 ].

Clinical signs and symptoms

Three dated studies documented the clinical presentation of human leptospirosis from culture-positive patients [ 41 , 42 , 68 ]. Common clinical presentations in increasing order were jaundice (5.9%), hepatomegaly (23.5%), meningism (23.5%), muscle tenderness (35.3%), respiratory tract manifestations (41.2%), rigour (41.2%), conjunctival injection (47.1%), digestive tract manifestations (58.8%), myalgia (58.8%), backache (64.7%), excess urobilin in urine (70.0%), joint pain (82.4%), headache (88.2%), abnormal urine deposits (90%), and albuminuria (90%).

Risk factors

Risk factors for exposure to leptospires both serologically and using PCR were either mentioned as likely risk factors due to higher positivity rates or estimated using univariable and multivariable models in 15 studies. In cattle, high seropositivity or odds ratios were observed in older animals [ 52 ], both males and females [ 22 , 52 ], grazing in communal sites [ 22 ], being near wildlife [ 22 , 23 ], and in larger herds [ 23 , 50 , 59 ]. Cattle, sheep and goats from areas with high rainfall amounts had high leptospiral seroprevalence [ 49 ]. Mature pigs and those kept with other species were also shown to have higher odds of seropositivity [ 61 ]. Mice were shown to have a higher occurrence of leptospires than rats by PCR [ 24 , 35 ]. Rodents from environments more conducive to harbouring leptospires, possibly due to factors such as reduced elevation, flooding risk, and proximity to rubbish dumps and drainages, had higher odds of testing positive by PCR in Nairobi’s Kibera informal settlement [ 35 ]. Lastly, migratory wildlife and free-ranging cattle were more likely to be seropositive than non-migratory and captive wild animals [ 39 ]. Seropositivity in humans was high in occupationally exposed slaughterhouse workers [ 20 ], pastoral farmers [ 26 ], and sugarcane workers [ 41 , 42 , 65 ].

Outbreaks and pathology studies

Outbreak investigations of animal leptospirosis were reported in cattle, pigs, sheep and goats [ 40 , 43 , 44 , 53 ] and an associated post-mortem investigation of cattle, sheep, goats, and pigs from the affected farms, experimental and natural infections was also found [ 69 ]. The main findings were nephritis with inconstant jaundice. A post-mortem investigation of canine leptospirosis not associated with any reported outbreak was found and was the earliest report of the disease in Kenya [ 70 ]. Icteric appearance of tissues, nephritis, hepatomegaly, splenomegaly, and enteritis were found in the infected dogs.

Human leptospirosis has been associated with outbreaks of acute febrile illnesses in pastoral communities in the former North-eastern province [ 25 , 71 ] and in patients in Malindi [ 72 ]. The largest known outbreak reported in humans was in Bungoma in the western region (referred to as “swamp fever” at the time) that caused several hospitalisations of school-going children and adults from surrounding communities, affecting more than 100 students and causing more than 30 casualties [ 73 – 77 ].

Leptospirosis awareness

Three studies on the knowledge, attitudes and practices surrounding leptospirosis were found, assessing the level of awareness in communities. These were one journal article and two PhD theses. An investigation in Nakuru revealed that only 18 out of 66 (27.3%) animal health service providers interviewed considered leptospirosis to be associated with bovine abortions, indicating low knowledge [ 78 ]. An assessment in Nairobi found that only 3.8% of clinical practitioners and laboratory personnel had suspected leptospirosis in their clinical practice. Additionally, only 2.3% would consider leptospirosis in the differential diagnosis of acute febrile illnesses of unknown origin. None of the health facilities surveyed in Nairobi (15/15, 100%) had the diagnostic capacity for MAT testing and rapid diagnostic tests (RDTs) [ 79 ]. Lastly, half (11/22, 50%) of pastoralist respondents interviewed in Laikipia and Maasai Mara (16/29, 55.2%) considered leptospirosis as a zoonotic disease that is not necessarily tick-transmitted, along with anthrax, brucellosis, helminthiases, trypanosomiasis and diarrhoeal diseases [ 80 ].

We present the first in-depth systematic review of human and animal leptospirosis in Kenya encompassing literature from 1951 to 2022. There was a spike in the publication numbers in the period 2010 to 2020. Most studies reported on the central, coastal, southern and western regions of the country. The vast arid and semiarid lands that are home to large populations of Kenya’s indigenous livestock kept in pastoral and agropastoral systems [ 81 ] and important wildlife ecosystems [ 82 ] were underrepresented. Studies mostly utilised serological methods to investigate antibodies against various serovars, leaving the genetic diversity of leptospires in Kenya largely unexplored. There is little awareness of leptospirosis among farmers, animal health and medical practitioners. Differing MAT panels and cut-offs were used leading to possible heterogenous results for the country, with the most common serogroup investigated being Icterohaemorrhagiae. Serovar diversity between humans, wildlife and domestic species did not significantly vary, suggesting similar environmental exposure across these epidemiological compartments and the need for more studies studying the transmission dynamics. The widespread presence of leptospires in various domestic animals, wildlife, and humans in various settings demonstrates the need for raising awareness in communities and among healthcare practitioners, and investments in diagnostics for more effective disease control and prevention.

A regional bias was observed, with most reported investigations situated in the central, coastal, southern, and western regions of Kenya, a probable leptospirosis risk profile of the country. The semi-intensive farming systems and relatively higher precipitation make these areas conducive transmission zones for leptospirosis. Urban centres such as Nairobi in the south-central region of the country have a burgeoning urban population and complex human-domestic-wildlife interfaces that facilitate bacterial transmission. However, large livestock populations exist in the arid and semi-arid eastern and northern regions of Kenya, along with communal grazing fields and the presence of rodents and wildlife which can all facilitate leptospiral transmission. Leptospira spp. were also implicated in outbreaks of acute febrile illnesses in human populations in these areas [ 25 , 71 ], justifying increased focus on these regions.

Several studies on leptospirosis in Kenya are out of date and utilised serology and culture, with animal inoculation to isolate the organism for diagnosis. The changing epidemiological landscape brought about by dynamic disease drivers such as climate change, urbanisation, agricultural intensification, population growth and land use changes necessitate up-to-date studies. These should focus on risk factors, circulating serovars, local strain diversity, and the transmission dynamics via a One Health prism to enable policy for rolling out adequate diagnostics, disease prevention and control measures. The increased awareness of non-malarial fevers after 2010 when the WHO recommended parasitological confirmation of malaria before treatment [ 11 ] could have led to renewed interest in leptospirosis research as demonstrated by the spike in journal articles and grey literature numbers.

Our review revealed that the country currently lacks adequate capacity for MAT testing, given that the test was more popular in studies before the year 2000. The only three studies that applied MAT testing from the year 2000 onwards were done in collaboration with laboratories with established MAT testing in Tanzania and Germany [ 34 , 61 , 63 ]. The MAT test is useful in determining infective serogroups which are important in clinical diagnosis and to understand the local epidemiological transmission of the disease. Vaccine development also currently relies on this information as immunity is relatively serovar-specific and vaccines should include homologous or antigenically-similar serovars to be effective [ 83 ]. However, cross-reactions between serogroups are common, and initial high titres against a noninfective serovar followed by high titres against the truly infective serovar (termed paradoxical reactions) are documented [ 83 ] and have been observed in small ruminants in Kenya [ 34 ]. Determining infective serovars can, therefore, be improved with repeat sampling. A challenge also exists in determining important serogroups to comprise a MAT panel. The commonly investigated serogroups of Icterohaemorrhagiae, Sejroe, Grippotyphosa, Canicola, and Australis were the most prevalent. Both the RGA and Ictero No.1 strains were used in some studies to represent Icterohaemorrhagiae because of their serological difference arising from an additional thermolabile antigen in Ictero No. 1 [ 84 ], thereby slightly contributing to the over-representation of the serogroup in MAT panels. Less included serogroups such as Djasiman could lead to underreporting, especially since the serogroup has been implicated in renal dysfunction in neighbouring Uganda [ 85 ]. Therefore, even though MAT testing has been utilised in the country for several years, there is a need for MAT panels that are as inclusive as possible to update Kenya’s information on circulating serovars, the resources available in a study notwithstanding. Lastly, the use of various MAT cut-offs can lead to heterogeneity between studies, making it difficult to compare studies in the country. The use of local strains in MAT panels can increase diagnostic sensitivity and has been recommended for African settings [ 86 ]. The WOAH recommends the use of reference strains of serovars, available from the WOAH reference lab [ 15 ], MAT cut-off titres of 1:100 and diagnosis of acute infection in animals be made with a four-fold rise in antibody titres between acute and convalescent serum samples [ 87 ]. The last study to culture for leptospires in Kenya was in the late 1980s, indicating a considerable gap in research efforts focussing on culturing and isolating leptospires from biological or environmental samples. Culture of leptospires can be performed for routine propagation of laboratory strains, or from clinical and environmental samples such as blood, cerebrospinal fluid, urine, livers, kidneys, water and soil using the EMJH media [ 88 ]. ELISA has also been used in the country but has been shown to have low diagnostic accuracy in endemic regions when compared to MAT when determining seroprevalence in humans [ 89 , 90 ], and may not always distinguish between vaccinated and infected cattle [ 87 ].

There is a severe lack of molecular investigations of leptospires, which are best placed to determine Leptospira species and characterise the bacteria according to its current WGS-based taxonomy. The earliest of the eleven PCR-based investigations found was from 2011, demonstrating a relatively recent adoption of molecular diagnostics in leptospirosis research in Kenya. The lipL32 target is commonly used to identify pathogenic leptospires (now sub-clade P1) [ 91 ]. However, the rrs gene is more sensitive in detecting leptospires in clinical samples due to the potential role of “intermediate” leptospires (now sub-clade P2) which lack the lipl32 locus [ 92 ]. A high prevalence of leptospirosis caused by these intermediates has been demonstrated in febrile patients in Ecuador, indicating their understated role in clinical disease [ 93 ]. Leptospira detection via PCR is typically done using loci that are present in all bacteria such as gyrB , rrs , and secY , or those found in pathogenic leptospires only such as lipL32 , ligA , ligB , and flaB with varying diagnostic accuracies being reported [ 92 , 94 ]. Strain diversity can be demonstrated using SLST, but multi-locus sequence typing (MLST) utilising housekeeping genes and the PubMLST database is robust in directly determining leptospiral genomospecies and illustrating local strain diversity. This approach has been fruitful in characterising novel strains in endemic countries [ 95 ]. Additional PCR methods such as viability PCR (vPCR) can identify live/intact leptospires from environmental samples [ 96 ], thus showing the added public health risk which can have application in disease surveillance in Kenya, especially when isolate recovery is not possible or successful. The utilisation of WGS on leptospiral strains offers unmatched resolution in determining the phylogenetic relatedness of isolates from various regions and determining pathogen characteristics such as sequence types, antimicrobial resistance genes, virulence factors, plasmid profiles, and serovars. Antimicrobial susceptibility testing of leptospiral isolates currently lacks official breakpoints for many antimicrobial agents, and the few studies performed show a lack of emergence of antimicrobial resistance for the bacteria [ 97 ].

Surveillance in diverse hosts is important in the country as most studies were focused on cattle, sheep and goats which are important reservoirs in the country. The pooled seroprevalence estimates found in cattle [ 98 , 99 ] were similar to other endemic countries, and those in goats were similar to those from Iran but lower than other estimates from Africa [ 98 , 99 ]. The heterogeneity observed was substantial, a likely result of the various diagnostic cut-offs, as well as other varying study characteristics. Future meta-analyses with more statistical power could undertake sub-group and meta-regression analyses to identify and characterise potential causes of between-study heterogeneity such as population demographics, study designs and geographical locations. This will enable harmonisation of studies in the country which can improve the comparability of results. Additionally, despite conducting a risk of bias assessment, our meta-analytic estimates are limited by the quality of the included studies and may be influenced by selection and publication bias. However, we did not attempt publication bias analyses due to the high heterogeneity found. Despite this, these analyses reveal a high but previously understated presence of cattle and caprine leptospirosis in the country. Efforts to reduce the disease prevalence in animals and increase productivity are crucial. Furthermore, the absence of comprehensive surveillance systems means the economic burden and contribution of human leptospirosis to febrile illnesses, as well as kidney, liver, neurological, respiratory, maternal and neonatal diseases, remain inadequately understood and likely underestimated.

Less or no focus was placed on rodents and various wildlife such as bats which could be important reservoirs as indicated by regional studies [ 100 ]. The few studies on dogs, pigs, and donkeys in the country give an unclear picture of the role of these hosts on leptospiral epidemiology in Kenya. Our investigation on the diversity of serovars in humans, domestic and wildlife revealed higher diversity in domestic animals that did not statistically differ from humans and wildlife. While the diversity measures used are sensitive to sample sizes [ 101 ], results obtained suggest similar environmental exposure of these three epidemiological compartments and the need for veterinary public health and One Health interventions to minimise exposure. Further research on the transmission dynamics of leptospirosis at the human-domestic-wildlife interface is needed to refine control options.

The risk posed to food vendors, consumers and others in the food value chain is largely unexplored in the country. A PCR-positive beef meat sample was found in grey literature [ 36 ] prompting curiosity about the uncommon finding and its implications for food safety. A high seropositivity of freshwater fish has been demonstrated in neighbouring Tanzania [ 102 ]. The use of slaughterhouse surveillance in studying leptospiral epidemiology can be a cost-effective way of screening animal/food samples with large geographical reach [ 103 ]. Studies on environmental samples are also lacking despite environmental exposure through occupations such as sugarcane farming and fishing being important risk factors in the country. Investigation of leptospirosis, which is an environmentally-driven zoonosis, extends beyond humans and animals and is best understood using a One Health approach that acknowledges the inter-relatedness of human, animal and environmental health. There is also a lack of estimates on the burden of animal leptospirosis and its incidence in important animal hosts such as cattle, with only one prospective cohort study found and revealing exceedingly higher incidence rates of small ruminant leptospirosis when compared to estimates in humans [ 34 ]. New approaches to estimating animal disease burden from the Global Burden of Animal Diseases program can help generate the burden of animal leptospirosis in Kenya which can guide policy and resource allocation [ 104 ]. Environmental drivers of the disease and the seasonality of human leptospirosis in Kenya are also largely undescribed, with the little current data showing a lack of seasonality of small ruminant leptospirosis [ 34 ]. However, recent work revisiting the 2004 outbreak of human leptospirosis in Bungoma shows that most cases occurred during or soon after the long rains (also MAM rains–March, April, May) [ 105 ]. Most investigations in this review were carried out in areas with higher precipitation, which may represent a risk profile of the disease in the country. However, reported cases can be utilised to develop spatio-temporal risk maps of leptospirosis that can help prioritise areas and seasons of increased leptospiral transmission in the country. Such risk maps can also incorporate data on temperature and rainfall patterns, thereby elucidating how future climate scenarios may impact the prevalence and geographic range of the disease.

Awareness of leptospirosis in farmers, animal health and medical practitioners was low. Additionally, it was demonstrated that several health centres are ill-equipped to diagnose leptospirosis due to the lack of RDT kits and infrastructure for MAT testing. While MAT is the serological gold standard that is useful in proving infective serogroups and determining the course of disease by agglutinating titres, it requires maintaining a panel of reference strains, dark field microscopes and knowledge of how to determine positives, making the interpretation subjective. This lack of diagnostic capacity can lead to undetected leptospirosis cases which can perpetuate a lack of awareness among health practitioners. There is a need for a tiered laboratory system to enable diagnostics in local and peripheral laboratories in high-risk areas using RDTs and the establishment of centralised reference labs for confirmatory tests, validation of diagnostics and to enable the country to participate in regional prevention and control efforts [ 106 ].

The clinical presentation of leptospirosis was non-distinguishing from the few studies that described the clinical signs and symptoms. Common clinical presentations for acute illness reported globally include fever, chills, headache, and myalgia. Conjunctival suffusion as an ocular manifestation is regarded as a distinguishing sign of human leptospirosis [ 4 ] even though it has been observed in patients with other infections such as Hantavirus [ 107 ], thus requiring careful consideration of the local epidemiological picture. Knowledge of the clinical signs and symptoms could be useful in syndromic surveillance, and future studies should determine the positive predictive values of various clinical signs and symptoms to inform policy that enables early clinical suspicion from health practitioners [ 108 ].

We found no official reports of prevention or control plans for leptospirosis in the country, even though a strategic plan exists for the prevention and control of zoonotic diseases with a One Health approach [ 109 ]. Prevention can be achieved through the use of personal protective equipment to prevent occupational exposure, protecting water and food sources from contamination from animal reservoirs, increasing awareness in communities to enable timely diagnosis, and controlling rodent infestations by clearing breeding sites such as garbage pits and improving sanitation [ 110 ]. Vaccination is a viable option for the control of animal leptospirosis and recent advances in vaccinology such as mRNA vaccines could hold the key to a universal leptospiral vaccine protective against a broad spectrum of pathogenic serovars [ 111 ], a prospect that could benefit from Africa’s growing capacity for producing advanced vaccines [ 112 ].

In conclusion, leptospirosis research spanning more than 70 years revealed a regional bias towards the central, coastal, southern and western parts of Kenya. Despite this, widespread exposure of leptospires was demonstrated in various hosts across the country. Moving forward, future research efforts should prioritise isolating and characterising the bacteria using molecular approaches. PCR-based tests offer a viable option for surveillance in humans, animals and the environment to characterise locally-circulating strains even when culturing for the bacteria is not possible or successful. This will enhance our understanding of the transmission dynamics in a One Health space. Additionally, investigating risk factors for exposure for various humans and animals, and paying attention to underrepresented reservoir hosts is essential for a more robust understanding of leptospiral epidemiology in Kenya. Efforts to implement rapid diagnostic tests for peripheral laboratories and MAT testing for central laboratories are vital for timely and accurate leptospirosis diagnosis. Lastly, raising awareness of leptospirosis among farmers, health practitioners and veterinary professionals is crucial for early recognition and diagnosis that can lead to effective management. Education initiatives targeting at-risk populations such as farmers and slaughterhouse workers can empower individuals with knowledge about risks, prevention and control strategies, thereby contributing to better public health outcomes.

Supporting information

S1 table. a summary of the characteristics of publications included in the systematic review..

https://doi.org/10.1371/journal.pntd.0012527.s001

S1 Data. Database search terms used to find literature on leading electronic databases.

The PRISMA checklist is also presented.

https://doi.org/10.1371/journal.pntd.0012527.s002

S2 Data. A summary of the data extracted from the 66 included studies.

https://doi.org/10.1371/journal.pntd.0012527.s003

Acknowledgments

We thank Matthias Flor for assisting in the R code for the alluvial diagram and Bernd-Alois Tenhagen for proofreading the manuscript. We also thank all researchers of the reports included in this systematic review.

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Scaling up public transport usage: a systematic literature review of service quality, satisfaction and attitude towards bus transport systems in developing countries

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Published: 26 September 2024

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Eugene Sogbe ORCID: orcid.org/0000-0002-9243-3481 1 ,
Susilawati Susilawati ORCID: orcid.org/0000-0003-1831-6743 2 &
Tan Chee Pin ORCID: orcid.org/0000-0003-0162-3763 3

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Urban sprawl driven by urbanisation has contributed to a sharp rise in privately owned vehicles and competition for restricted resource space. The utilisation of private vehicles has increased, particularly in developing countries, and this phenomenon leads to many negative externalities, including traffic congestion and emissions. To encourage the use of sustainable modes such as public transport, it is essential for policymakers and transport authorities to carefully examine the determinants influencing public transport usage and apply successful policies and procedures. This review offers a valuable understanding of the contemporary knowledge regarding the determinants influencing bus transport usage. It systematically reviews 104 papers published since 2000 on service quality, satisfaction, and attitudes towards bus transport. The review shows that safety, security, comfort, reliability and accessibility are the most substantial determinants shaping users' views on service quality and satisfaction. This is particularly evident in situations like waiting at the bus stop, being on board the bus, and specific instances while walking to their destination. The results indicate that challenges with first-mile and last-mile connectivity are apparent, and further exploration in the context of developing countries is needed to understand these challenges, necessitating further investigation. It also demonstrates instrumental aspects such as convenience and social-symbolic aspects such as social standing, influencing attitudes towards public transport usage. It concludes by suggesting potential paths for future research and discusses the impacts of the results on policy decisions.

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1 Introduction

Urban sprawl driven by urbanisation has contributed to a sharp rise in privately owned vehicles and competition for restricted resource space (Yu et al. 2019 ; Li et al. 2020a ). Too many private vehicles on the road network lead to negative externalities, including congestion and emissions. Several of these external effects linked to the heightened utilisation of private vehicles can be addressed by reducing their usage to more viable modes of transport, like public transport (hereinafter, PT). Prior studies have documented the merits of using PT for individuals and cities through the promotion of good health, energy conservation and emission reduction, reduction in vehicular accidents, traffic congestion reduction, and provision of jobs (Nguyen-Phuoc et al. 2021 ; Cheranchery and Maitra 2018 ; van Soest et al. 2020 ; Truong and Currie 2019 ).

PT has experienced a decrease in usage in recent times (Boisjoly et al. 2018 ; Miller et al. 2018 ). This decline was exacerbated when many countries battled the COVID-19 outbreak (Jenelius and Cebecauer 2020 ; Sogbe 2021 ; Tirachini and Cats 2020 ). A decrease in PT usage is caused by many factors, including the built environment (BE), public policy, extent of economic development, and acquisition and utilisation of privately owned vehicles (Zhang et al. 2022 ). However, de Oña ( 2021 ) noted that service quality (hereinafter, SQ), satisfaction and behavioural intention or attitude towards PT are three crucial factors influencing a mode shift. Poor SQ (e.g., reliability, comfort) leads to a satisfaction gap and, subsequently, a negative attitude towards PT (Cheranchery and Maitra 2018 ). Thus, passengers’ satisfaction with PT and the ability to entice new users through a mode shift hinges on the quality of service (van Lierop and El-Geneidy 2016 ). This suggests that knowing the dimensions of PT usage and improving on them can mitigate the acquisition and use of private vehicles, which are competitors to PT and threats to the environment and human survival.

Pourbaix ( 2011 ) estimated an 80% global increase in daily urban travel using private vehicles by 2025, with the growth occurring in developing countries. Similarly, the World Health Organization ( 2011 ) noted that private vehicle usage in emerging countries is expected to supersede that of developed nations by 2030. Recent studies have confirmed these earlier projections (Saxena and Gupta 2023 ; Soltani 2017 ; Ntim et al. 2022 ). Besides, travel requirements in emerging and developed nations may differ due to differences in vehicle ownership, transport systems, infrastructure, and economic status. It is, therefore, necessary to apply successful policies and procedures to increase PT usage. However, this requires a thorough understanding of extant knowledge, clear-cut lacunae, and disagreements that must be resolved. Policymakers and transport authorities may lack the knowledge to make informed judgments without a complete and systematic research evaluation.

As far as we know, no systematic literature review focused on these three factors influencing PT usage. In a prior review, Das and Pandit ( 2013 ) reviewed aspects of bus transport service that impact users' perceived quality of service. This contributed significantly to the SQ factors that define the level of service of PT. However, while their study emphasised service factors, it did not provide a clear-cut methodology, and the selected literature is not exhaustive. de Ona and de Ona ( 2015 ) presented a review of SQ, providing an extensive review of methodologies deployed in the study of SQ and the merits and demerits of the methods. However, it focused more on the methodologies than the SQ attributes. Besides, most selected papers focused on SQ in the aviation industry. van Lierop et al. ( 2018 ) analysed important factors (i.e., satisfaction and loyalty). Their study provided insights into the features that encourage PT users to remain committed to using it. However, the scope of their review was limited by geographical boundaries, with only two papers from Africa and Asia each. Ojo ( 2019 ) subsequently provided a literature review of SQ attributes and the methodologies deployed. It highlighted the need to identify important attributes concerning the type of PT, regional context, and culture. However, the study limited the review to 2015; therefore, information about SQ from 2016 to the publication date, 2019 and subsequent years have been excluded.

This study aims to systematically review and examine existing literature on the attributes influencing PT usage, focusing specifically on three important factors: SQ, satisfaction and attitude towards PT usage within the context of developing countries to address the specific needs and concerns of passengers. It identifies and discusses the attributes based on qualitative (subjective) and quantitative (objective) assessments and the impact on the utilisation of PT. It should be mentioned that this research focused on public buses, including bus rapid transit (BRT), as these modes of transport are dominant and synonymous with most developing countries (Nguyen-Phuoc et al. 2021 ; Cheranchery and Maitra 2018 ).

The ensuing sections of this paper are structured as follows: Sect. 2 , which contains the methodology, provides the scope of the review and presents the strategy for the systematic literature search and selection. It is followed by Sect. 3 , which presents the results and the influence of SQ, satisfaction, and attitude towards PT usage. Section 4 offers future research directions and policy implications, including a synopsis of the evidence.

2 Methodology

The study adopted a systematic literature search using the Preferred Reporting Items for Systematic Reviews and Meta-Analysis (PRISMA) guidelines (Moher et al. 2015 ). The search was done in January 2023 and updated in July 2023. The data source repositories were TRID: TRIS and ITRD, Scopus, Web of Science, Inspec, Compendex and GeoBase. Having identified the keywords following an exploratory review, a search using Boolean operators was carried out:

(“public transport” OR “public transport usage” OR ridership) AND (factors AND “developing country”).

2.1 Inclusion and exclusion criteria

The criteria for including or excluding selected papers in the systematic review were as follows:

Papers were included if they focused on research conducted in developing countries.

Papers not in English were excluded.

Papers related to COVID-19 and PT were excluded. The study recognises the broader context of declining PT usage and the concurrent rise in private car usage in developing countries, as highlighted in the literature even before the pandemic outbreak. Moreover, it is essential to emphasise that while COVID-19 has undoubtedly impacted PT usage patterns in the short term, it is transient, and its long-term implications are uncertain. It is possible that some changes observed during the pandemic, such as increased remote work and a preference for private transportation to maintain social distancing, may persist to some extent even after the pandemic has subsided. However, historical trends suggest that PT remains a vital component of urban transportation systems, and factors such as population growth, urbanisation, environmental concerns, and congestion will continue to drive demand for efficient PT solutions. Therefore, while COVID-19 may have influenced PT usage patterns in the short term, its long-term impact remains to be seen, and other factors, such as SQ, satisfaction, and attitude towards PT, are most likely to play a significant role in shaping future trends.

Papers that combined SQ and satisfaction of various modes, including paratransit, were excluded.

Only peer-reviewed research or journal articles were included.

Papers on SQ, satisfaction, and attitudes towards public bus transport, including BRT in developing countries, were included. This is because bus transport is a widespread means of transportation synonymous with many developing countries.

Papers published between 2000 and 2023 were considered.

The search in the repositories mentioned above yielded the following results: TRID: TRIS and ITRD (15,000), Scopus (32,010), Web of Science (3752), Inspec (1603), Compendex (2012) and GeoBase (1558). Further details of the search process and results are provided in Table 1 and Fig. 1 . This resulted in a total of 55,935 articles gathered, with subsequent field restrictions applied, leading to 2483 records (refer to Table 1 ). This number was imported into Rayyan (Ouzzani et al. 2016 ), and 962 duplicates were removed, leaving 1521 records. The authors then screened titles and abstracts to determine whether they focus on (i) SQ and satisfaction with public bus transport and (ii) attitudes towards PT. The inclusion and exclusion criteria are listed above. This was done to narrow the selection to articles aligned with the topic, resulting in 335 chosen for full-text review. Of these, 13 articles were unavailable, leaving 322 for full-text review. In the full-text review, 92 records were excluded for lacking relevance to the research theme, 67 for combining SQ and satisfaction of different modes, 35 for focusing on paratransit and related modes, and 30 for concentrating on the built environment as a factor. The snowballing method identified 10 additional studies from reference lists, of which 6 were retained following the same criteria. The systematic search produced an extensive body of literature on the subject, with a final selection of 104 papers for the review. The PRISMA flow diagram in Fig. 1 depicts the number of records at each stage and the reasons for exclusion and inclusion.

PRISMA flow diagram

Various pieces of information were documented from each of the records. Initially, general details, including author(s) and publication year, were extracted to provide the research’s context and scope. Subsequently, we scrutinised the methodologies employed for data analysis (such as SEM), the data source (primary or secondary), approaches for collecting data (such as questionnaires or interviews), and the sample size. Finally, data were compiled on the constructs that were assessed.

3.1 Patterns in literature

China leads in publications, accounting for nearly a quarter of all studies (23), followed by India with under one-fifth (18), Brazil (7), Ghana (6), Vietnam (5), Bangladesh (6), and Ethiopia (6). Other countries collectively share the remaining research. Azerbaijan is transcontinental, with 1 study and 1 review article focusing on developing countries. It is evident that research predominantly centres on Asian countries, and there is a dearth of research in developing nations beyond Asia. These countries can potentially introduce fresh perspectives to the research on the subject. Figure 2 illustrates the publication count by country, while Fig. 3 shows the geographical distribution.

Distribution of publications by country (by July 2023)

Distribution of publications by continent (by July 2023)

3.2 Methodological approaches and empirical findings in PT research

The articles in this literature review utilised qualitative and quantitative data and data analysis methods. Quantitative data involves collecting data through surveys, experiments, or statistical analysis. On the other hand, qualitative data provides insights into attitudes, opinions, behaviours, or motivations and is often gathered through interviews or observations. The plurality of studies analysed in this review relied solely on quantitative data (98). In two cases, qualitative data was used. Mogaji and Nguyen ( 2021 ) utilised semi-structured interviews to investigate the level of contentment of passengers with disabilities. In addition, Simangunsong et al. ( 2023 ) used interviews to assess the perception of BRT users. In four cases, qualitative data was integrated with quantitative data. Thai and Quan ( 2023 ) combined interviews and surveys to analyse the determinants influencing urban individuals' inclination to utilise buses. Kacharo et al. ( 2022 ) studied the safety and security of female passengers using focus group discussions and questionnaires. Araya et al. ( 2022 ) combined a questionnaire survey, ethnographic observations and document reviews to evaluate the safety and security of women on public buses. Finally, Busco et al. ( 2023 ) examined the connection between bus transport and social exclusion using surveys and focus group discussions. The majority of studies relied on primary data sources (94); however, a few utilised secondary sources, including data gathered by transit agencies (7) or initially gathered for different research projects (3). The primary method of data collection in most cases was through questionnaire surveys.

There are vast differences in sample sizes, with the least being 29 respondents from a questionnaire survey (Ganji et al. 2021 ) and the highest being 588,000 from a transit agency entry data (Guzman et al. 2019 ). Common analysis methods deployed include the service quality (SERVQUAL) model and service performance (SERVPERF) model, which have been widely used, structural equation modelling (SEM), importance performance analysis, different kinds of regression analysis and machine learning algorithms such as random forest (RF) and gradient boost decision trees (GBDT).

While most studies leaned towards quantitative analysis, a few incorporated qualitative data, demonstrating a balanced exploration of the subject matter. Moreover, the range of sample sizes across studies underscores the diversity in research approaches, from smaller-scale surveys to extensive transit agency data analysis. This variation reflects the complexity and breadth of the topic under investigation, accommodating different methodological requirements and research objectives. A spectrum of techniques was employed in terms of analysis methods. The diversity of research methodologies and analytical approaches showcased in the literature contributes to a comprehensive understanding of PT usage dynamics and SQ assessment. Researchers can glean valuable insights into the complex interplay between SQ, passenger satisfaction, and mode choice behaviour by exploring qualitative and quantitative findings.

The literature debates the best possible methodology for examining SQ dimensions and satisfaction. The SERVQUAL model established by Parasuraman et al. ( 1985 ) measures commuter differences in appreciation and expectation of SQ dimensions. Nonetheless, Cronin and Taylor ( 1992 ), as cited by Esmailpour et al. ( 2020 ), highlighted that the measure of commuters' expectations is not of the essence and, in lieu, put forward the SERVPERF model, which utilises performance perception to measure SQ. Matzler et al. ( 2004 ), cited by Zhang et al. ( 2019a ), highlighted that, albeit salient, IPA has a linear and symmetric association between satisfaction as a dimension and satisfaction in general, which they claimed is a distorted supposition. The authors made a case for the three-factor theory as a better alternative to eliminate distortions.

Similarly, Tuan et al. ( 2022 ) indicated that the IPA has crucial conceptual and methodological constraints, favouring the three-factor theory. Zheng et al. ( 2022 ) made a case for the three-factor theory, arguing that the other methods, including linear regression, are flawed because they presume linearity and symmetricity for SQ dimensions. Fang et al. ( 2021 ) shared the same viewpoint concerning IPA; however, by contrast, they added that the three-factor theory also has the same weakness as IPA in determining the hierarchy of significance of commuter satisfaction and, therefore, proposed GBDT and Impact Asymmetry Analysis (IAA).

3.3 Identifying qualitative and quantitative factors that impact perceptions of SQ and satisfaction

Over time, researchers have employed a broad array of factors to examine the utilisation of PT. Among these, SQ and satisfaction encompass a vast number of studies. In this section, we present a summary of these factors, which were informed by qualitative and quantitative assessments, and their impact on utilising bus transport.

Nathanail ( 2008 ) posited that the SQ of PT is assessed through two leading indicators. The objective indicator, provided by operators, is a quantitative metric for comparison with standards or past performance. The subjective indicator, derived from surveys, offers qualitative measures, capturing users' perceptions by evaluating the gap between actual and ideal service levels. Quantitative factors are typically measured using numerical data. For example, frequency—quantifying the regularity and frequency of PT services, indicating how often vehicles are available, travel time—assessing the duration it takes PT vehicles to travel between stops or destinations, etc. and qualitative factors involve subjective assessments of availability or passenger comfort. Although these two measures exist, a plurality of the studies employed qualitative factors. On the other hand, very few researchers have focused on measuring these factors quantitatively. The SQ and satisfaction factors that significantly impact PT usage overlap. Nonetheless, we discuss them separately for clarity.

Cronin and Taylor ( 1992 ) defined SQ as “an attitude that reflects a comprehensive, long-term evaluation.” Parasuraman et al. ( 1985 ) provided a historical definition of SQ: “SQ perceptions result from comparing consumer expectations with actual service performance.” This has led to the widely embraced perspective that excellent SQ entails delivering performance that either meets or surpasses customers' expectations of the service. Commuter perception constitutes a crucial aspect of SQ. In our analysis, 47 papers assessed commuters’ perception of SQ. Most papers examined SQ with various factors, such as availability, reliability, safety, security, cleanliness, etc. Table 2 summarises the literature on SQ, which is incorporated in this review.

Two factors that featured prominently in most papers in the review are the perception of passengers regarding their safety (30) and security (19) during transit, with one paper each considering quantitative insights. The authors asserted that safety and security are the most influential determinants of public bus usage and are strongly associated with gender (Ikhlaq et al. 2017 ; Alomari et al. 2023 ; Suman et al. 2016 ; Deb and Ali Ahmed 2018 ; Houria and Farès, 2019 ; Adom-Asamoah et al. 2021 ; Nguyen-Phuoc et al. 2021 ; Busco et al. 2022 , 2023 ; Araya et al. 2022 ; Kacharo et al. 2022 ; Verma et al. 2020 ). Safety and security have an overarching impact on other latent attributes (Wang and Zhu 2014 ), and this is reflected while on-board the bus (Hu et al. 2015 ; Orozco-Fontalvo et al. 2019 ; Yarmen and Sumaedi 2016 ) or while waiting at the bus stop or station, especially at night (Busco et al. 2022 ; Esmailpour et al. 2020 ; Suman et al. 2016 ; Noor and Iamtrakul 2023 , 2024 ). Addressing safety and security concerns is vital for building public trust, encouraging ridership, and creating a positive experience for passengers using PT.

Another significant qualitative factor in this review is service reliability (20), with 19 papers measuring qualitative aspects. Chakrabarti and Giuliano ( 2015 ) defined reliability “as one which consistently operates according to its schedule or plan.” The varying aspects of this factor complicate it. For example, the arrival and departure of PT may be timely, but disparities in the dwell time over the period may lead to delays and impact schedule adherence, potentially affecting the reliability of the service about meeting predetermined schedules. While timely performance significantly influences passengers’ use of bus services (Deepa et al. 2022 ; Cheranchery and Maitra 2018 ; Randheer et al. 2011 ; Sam et al. 2018 ; Das and Pandit 2015 ), in-vehicle time poses a significant obstacle to the use of bus services (Maitra et al. 2015 ; Thai and Quan 2023 ; Shen et al. 2016 ). In-vehicle time refers to the duration passengers spend travelling inside the bus or other PT vehicles. This time spent in transit can significantly influence passengers' decisions regarding bus services. Factors such as longer travel times or perceived inefficiencies during the journey can pose obstacles or challenges that may deter individuals from utilising bus services. Therefore, understanding and addressing issues related to in-vehicle time is crucial for improving the attractiveness and efficiency of bus services. In addition, waiting time indirectly impacts passengers’ perception of the reliability of PT (Hu et al. 2015 ; Chaudhary 2020 ; Fu et al. 2018 ). As demonstrated through the various studies, a reliable PT system contributes to increased ridership and positively impacts overall transportation behaviour. The ability of PT to adhere to schedules, provide consistent service, and minimize disruptions plays a pivotal role in shaping users' perceptions and preferences. Addressing and improving reliability issues can be crucial for promoting PT's widespread and sustainable use.

Affordability as a qualitative factor involves the assessment of user perceptions of the cost of PT services. In our review, 16 papers examined affordability, with twelve considering qualitative insights. The authors opted for varied terminologies to label this attribute. Most authors measured affordability as fare (6), cost or coined travel cost (7), ticket price (2), pricing or price (2) and affordability (1). Many PT users view affordability as a deciding factor. A principal reason for using PT is low bus fares (Kacharo et al. 2022 ; Birago et al. 2017 ; Alomari et al. 2023 ; Sam et al. 2014 ) and an increment in transport fares engender a decrease in PT usage (Maitra et al. 2015 ; Joewono et al. 2016 ; Adom-Asamoah et al. 2021 ) and low-income earners are the hardest hit by the increases (Toro-González et al. 2020 ). This indicates that for most passengers, the use of PT is contingent on affordability.

In 14 papers, the authors asserted that commuters’ perceived comfort is a significant driver of PT usage. Some of these papers examined the overall influence of comfort on PT usage and its association with in-vehicle crowding (Saleem et al. 2023 ; Sam et al. 2014 ; Deepa et al. 2022 ; Thai and Quan 2023 ; Atombo and Wemegah 2021 ; Birago et al. 2017 ; Houria and Farès, 2019 ; Adom-Asamoah et al. 2021 ), in-vehicle comfort, precisely seating comfort, the temperature inside the bus and facilities at the station (Deb and Ali Ahmed 2018 ; Shen et al. 2016 ; Alomari et al. 2023 ; Esmailpour et al. 2020 ; Hu et al. 2015 ). In our review, eight papers evaluated crowdedness in the bus or at stations (Shen et al. 2016 ; Deb and Ali Ahmed 2018 ; Maitra et al. 2015 ; Chaudhary 2020 ). Shen et al. ( 2016 ) highlighted that crowdedness substantially influences commuters’ perception of comfort and has a more pronounced effect on commuters standing than those seated.

In our review, 16 papers measured accessibility, with nearly all (13) considering qualitative insights. Aspects considered include the ease with which passengers can navigate PT systems, such as information availability or ease of use (Busco et al. 2023 ; Houria and Farès, 2019 ; Ikhlaq et al. 2017 ). Other qualitative factors include cleanliness inside the bus and seats (8) (Deepa et al. 2022 ; Chaudhary 2020 ; Saleem et al. 2023 ; Hu et al. 2015 ; Birago et al. 2017 ), availability (9) (Adom-Asamoah et al. 2021 ; Hu et al. 2015 ; Atombo and Wemegah 2021 ), driver behaviour, speed and customer care.

Regarding quantitative factors, three papers measured accessibility by considering aspects such as service coverage (Insani et al. 2021 ) and the number of vehicles in service (Toro-González et al. 2020 ; Rabay et al. 2021 ). Challenges with transfers, access and egress modes can deter commuters from using PT. Insani et al. ( 2021 ) noted that switching between buses contributes to extended travel time, posing a distinct drawback for PT users, and integration with other modes of PT is recommended. Toro-González et al. ( 2020 ) concluded that increasing the number of vehicles in operation results in a rise in PT demand. Nonetheless, this depends on the speed of the vehicles. Four papers measured affordability (Guzman et al. 2019 ; Rabay et al. 2021 ; Toro-González et al. 2020 ; Insani et al. 2021 ). One paper each measured indirect aspects of reliability and frequency of PT; Insani et al. ( 2021 ) measured waiting and travel time, while Toro-González et al. ( 2020 ) measured the frequency of arrival and departure.

Other researchers advocated and used a combination of qualitative and quantitative assessments. Combining these measures could offer a more practical and dependable tool for assessing transit SQ (de Ona and de Ona 2015 ). In our review, two papers used both measures to assess commuters’ perception of SQ and satisfaction. Rong et al. ( 2022 ) measured perceived and actual time-related factors such as stopping, dwell, waiting, and travel times. In addition to time-related factors, Suman et al. ( 2016 ) measured connectivity, cost, security, punctuality, accessibility, comfort and safety.

3.3.1 Satisfaction

While SQ involves a cognitive assessment of the variance between initial expectations and perceived performance, satisfaction is its emotional equivalent. It pertains to the customer's contentment or dissatisfaction with the service (Carvalho Dos Reis Silveira et al. 2022 ). Table 3 shows a summary of the literature on satisfaction, which is incorporated in this review. In our review, 52 papers examined commuters' satisfaction with PT usage. Virtually, all the papers used a range of service factors, such as accessibility, reliability, and cleanliness, to mention a few. In some instances, we observed that alternative factors like passenger expectation (2) and perceived value (2) were considered satisfaction factors. Also, mood, emotions and cognitive activities (1) were used as satisfaction attributes. In urban environments characterised by high population density and extensive PT networks, factors influencing commuters' satisfaction with PT services are of paramount importance. Geographical nuances, social dynamics, and the nature of PT offerings are pivotal in shaping passengers' experiences and perceptions.

Commuters face many challenges when utilising bus transport across diverse urban landscapes, from bustling metropolises to smaller urban centres. Accessibility is critical, particularly for individuals with disabilities or mobility limitations. Ramps for wheelchairs (Ali and Abdullah 2023 ; Ji and Gao 2010 ), accessible stations (Jayakumar et al. 2023 ; Chaisomboon et al. 2020 ; Girma 2022 ), information accessibility regarding signage about routes, schedules, and facilities (Nguyen and Pojani 2023 ; Han et al. 2022 ; Girma et al. 2022 ), information regarding announcements to inform passengers about stops, transfers, and other relevant information (Fang et al. 2021 ; Lan et al. 2022 ; Fu and Juan 2017) and technological accessibility regarding real-time information through apps or displays, assisting passengers in planning their journeys (Mendez et al. 2019 ; Bose and Pandit 2020 ; Li et al. 2020b ). These are essential elements ensuring inclusivity and ease of use for all passengers.

In the rapidly urbanising environments of developing countries, where PT infrastructure may be limited and urban congestion is common, the comfort of passengers during their transit journeys becomes paramount. Factors such as comfort while waiting and riding (Githui et al. 2009 ; Zhang et al. 2019b ; Nwachukwu et al. 2019 ; Tuan et al. 2022 ), the temperature in the bus (Wu et al. 2016 ; Freitas 2013 ), seating comfort (Andaleeb et al. 2007 ; Githui et al. 2009 ) and ventilation (Esmailpour et al. 2020 ), and the condition of vehicles (Umme et al. 2022 ; Singh 2016 ) significantly influence passenger satisfaction. The qualitative insights gleaned from 32 examined papers shed light on how these comfort-related factors impact passenger perceptions and contribute to their overall satisfaction with bus transport services. Studies conducted by Andaleeb et al. ( 2007 ), Allen et al. ( 2019 ), Nwachukwu et al. ( 2019 ), and others highlighted the tangible effect of improved comfort measures on passenger satisfaction, emphasising the importance of addressing these factors within the unique context of developing country urban settings.

Furthermore, safety and security concerns loom large in commuters' minds, influencing their overall satisfaction with bus transport. Whether waiting at a bus stop (Sun et al. 2020 ; Zhang et al. 2019a ) or navigating through crowded vehicles (Ali and Abdullah 2023 ), passengers prioritise their well-being and peace of mind. Enhancing safety measures and providing a secure environment can significantly improve the attractiveness of bus transport services.

Affordability is another pressing issue, especially in urban areas where the cost of living may be high. Passengers evaluate the financial accessibility of bus transport services, weighing fares against their budgetary constraints. As such, pricing strategies and fare structures are pivotal in shaping commuters' perceptions of affordability and satisfaction.

In addition to these qualitative factors, quantitative metrics such as reliability, comfort, and availability also come into play. On-time performance, seating comfort, and frequency of services directly impact passengers' experiences and satisfaction levels. PT operators must maintain high standards across these dimensions to meet urban commuters' diverse needs and expectations. Table 4 shows the categorisation of qualitative and quantitative factors influencing satisfaction.

3.4 Attitude towards PT

Private car ownership and usage are often considered deterrents to PT utilisation. Reza Jalilvand et al. ( 2012 ) highlighted that a person's attitude influences their actions, and the theory of planned behaviour (TPB) suggests attitudes impact behavioural intentions (Ajzen 1991 ). Scholars have thus explored the attitudes and intentions of non-PT users, particularly private car users. Social-symbolic, affective and instrumental aspects influence the acquisition and use of cars (Gatersleben 2007 ). In our review, the papers on attitudes towards PT usage are scanty, and most travel behaviour research to date has primarily centred on instrumental aspects. Table 5 shows a summary of the literature on attitudes towards bus transport usage, which is incorporated in this review.

Four papers focused on instrumental aspects, while one paper focused on social-symbolic aspects. The instrumental aspects assessed include cost, flexibility, safety, reliability, travel time, direct lines, comfort, speed and convenience (Tao et al. 2019 ; Al-Ayyash and Abou-Zeid 2019 ; de Magalhães and Rivera-Gonzalez 2021 ; Li et al. 2019b ) and social-symbolic aspects such as success and status (Li et al. 2019a ). The intention of car users to use PT is considerably influenced by cost, reliability, comfort, travel time, and connectivity and enhancing these factors will boost the intention to use PT (Li et al. 2019b ; de Magalhães and Rivera-Gonzalez 2021 ).

In addition to understanding the factors influencing attitudes towards PT usage, it is crucial to consider the implications of these attitudes for PT policy and planning. For instance, emphasising instrumental aspects such as cost, reliability, and comfort highlights the importance of improving SQ to encourage PT adoption among private car users. Similarly, the recognition of social-symbolic aspects, such as perceptions of success and status associated with car ownership, underscores the need for targeted marketing and messaging campaigns to challenge prevailing cultural norms and promote the social desirability of PT usage. By addressing instrumental and social-symbolic factors, policymakers and urban planners can develop more effective strategies to incentivise PT usage and reduce reliance on private cars.

3.5 Evolution and trends in PT SQ and satisfaction research

Until the last two decades, few studies on PT SQ and satisfaction were conducted in emerging countries. The rapid growth of urban populations and increased income levels resulting from economic improvement generated a significant demand for individual mobility, hence the increased need for assessing this subject.

According to our review, the service factors influencing PT usage investigated over the decades are no different from those assessed today except for a few variations and additions. Before 2020, the investigation predominantly involved qualitative assessments of SQ and satisfaction factors. Since 2020, there has been a shift towards quantitative assessments, including accessibility, reliability, affordability, and transfers.

Since time immemorial, SQ factors like cleanliness, accessibility, reliability, comfort, affordability, etc., have been used in assessing SQ. However, in the last couple of years, researchers introduced factors which impact service reliability into the analysis, such as frequency, waiting time, turning frequency, stopping frequency, travel time, arrival interval, on-time performance, punctuality, information and transfer convenience.

The methodology for data collection and data analysis on the subject has also evolved from SERVQUAL and SERVPERF models and descriptive statistics (Aniley and Negi 2010 ; Randheer et al. 2011 ) to more robust methods such as SEM and ML algorithms like GBDT and RF (Nguyen-Phuoc et al. 2021 ; Lan et al. 2022 ; Fu 2022 ). With technological advancements, different data collection methods have been adopted, such as using social media, ticketing data, PT data, and automatic vehicle location (AVL) data (Rong et al. 2022 ; Suman et al. 2016 ; Tavares et al. 2021 ; Zheng et al. 2021 ; Rabay et al. 2021 ).

An emerging trend involves examining the preferences of different commuter groups. The extant literature revealed disparities in the desired quality and satisfaction of SQ dimensions among PT users. This diversity among commuters has led researchers and practitioners to emphasise heterogeneity in the PT market. Segmenting commuter groups can help transport authorities provide tailored services to meet the satisfaction of specific user groups (Allen et al. 2019 ) and allocate resources effectively for targeted interventions (Fu 2022 ). Our review revealed that such disaggregation has been chiefly conducted for youth, students, tourists, groups considered vulnerable (such as older people, women, and people with disabilities, PWD’s) and more recently, for captive and choice riders.

Based on the scarce literature available regarding segmentation according to elderly passengers, it can be inferred that elderly passengers’ satisfaction is greatly influenced by station broadcast, driver’s habit, punctuality, awnings, complaint handling, safety and security, driver courtesy, information services, waiting time with station broadcast being the most important (Yuan et al. 2019 ; Chaisomboon et al. 2020 ; Lan et al. 2022 ; Busco et al. 2023 ). Moreover, older public bus users encounter deficiencies in bus stop infrastructure, accessibility and information (Busco et al. 2023 ).

Researchers have explored segmentation based on the frequency of PT usage, dividing commuters into frequent and occasional riders. Fang et al. ( 2021 ), Tuan et al. ( 2022 ), Cheranchery and Maitra ( 2018 ) and Maitra et al. ( 2015 ) investigated the relationship between bus service dimensions and overall satisfaction for both rider groups. Aside from finding notable variance in how these groups perceived SQ, they found dimensions both groups prioritise in common: availability and accessibility (Tuan et al. 2022 ), waiting area, driver's behaviour, complaint handling, stop announcements (Fang et al. 2021 ).

Concerning students, diverse factors influence their satisfaction with PT. Agyeman and Cheng ( 2020 ) found that frequent breakdowns and extended travel times hinder school bus transport, affecting pupils' learning environment, while for university students, reliability and punctuality are of concern when using public buses (Javid and Al-Kasbi 2021 ). Furthermore, fare, comfort, reliability, and safety are vital attributes that impact the choice of PT (Sam et al. 2014 ) and fear of sexual harassment caused female students to avoid public buses (Nguyen and Pojani 2023 ). Jomnonkwao et al. ( 2022 ) switched the scope slightly by focusing on parents' perceptions of school bus SQ, highlighting that infrastructure, information, and safety dimensions influence their views.

Regarding youth commuters, there is proof that enhancing factors like performance, comfort, and assurance would boost satisfaction among youth PT passengers. What’s more, Busco et al. ( 2023 ) concluded that young PT users lack safety and SQ and face issues of harassment on PT systems. Nwachukwu et al. ( 2019 ) are the sole researchers who examined tourists' satisfaction. According to their results, tourists are discontent with PT usage, citing several SQ factors, particularly accessibility.

In our review, only two papers investigated the travel satisfaction of disabled travellers. Mogaji and Nguyen ( 2021 ) found gender-based disparities in travel satisfaction, noting that disabled women's satisfaction was more influenced by security, vulnerability, and the need for assistance compared to disabled men, while high floors in PT vehicles, crowded conditions, and untrained staff are factors affecting PT usage for people with disabilities (Ali and Abdullah 2023 ). Moreover, they also emphasised the lack of sufficient space for mobility aids in PT as a prominent challenge.

The segmentation also considered the viewpoint of female commuters. From the literature, safety and security are major quality issues and a significant barrier to public bus usage, given that a substantial portion of women experiences sexual molestation and psychological and physical violence often perpetrated by conductors and male co-passengers on buses and at bus stops (Busco et al. 2023 ; Saigal et al. 2021 ; Kacharo et al. 2022 ; Verma et al. 2017 ; Orozco-Fontalvo et al. 2019 ; Araya et al. 2022 ; Umme et al. 2022 ). In a recent review, Noor and Iamtrakul ( 2023 ) highlighted the prevalence of harassment on PT and the lack of responsive policy support to address this issue in developing countries. Figure 4 shows a schematic representation of the evolution and trends in PT SQ and satisfaction research in developing countries.

Evolution and trends in PT SQ and satisfaction research in developing countries

4 Future research directions and policy implications

4.1 synopsis of the evidence.

The results in Sect. 3 reveal that using PT for commuting is affected by various SQ factors, satisfaction-related aspects, and attitudes. These effects span pre-commute, commute, and post-commute phases. We highlight the attributes which have been discussed in this literature review.

Safety and security stand out as one of the crucial dimensions influencing users' perception of SQ and satisfaction. This finding contrasts with van Lierop et al. ( 2018 ) conclusions, who concluded that safety is not such a strong indicator of satisfaction in developed countries like those in Europe.

Commuters’ perception of reliability also correlates with usage and satisfaction. Overall, this aspect wields a substantial impact on satisfaction. This observation is consistent with the findings of van Lierop et al. ( 2018 ), who highlighted that enhancing the onboard experience is only advantageous if passengers are content with the service's reliability. On the other hand, comfort is a crucial factor during both the pre-commute and commute phases.

The convenience of individuals accessing and using PT services is crucial in determining PT systems' overall effectiveness and inclusivity. Accessibility, according to the review, is among the most critical attributes that impact satisfaction. Improving accessibility in PT is essential for creating a system that is convenient, equitable, and capable of meeting the population's diverse needs.

Affordability is another important factor. Many PT users are motivated by its affordability, and any rise in cost disproportionately affects individuals in the lower income brackets (Adom-Asamoah et al. 2021 ).

Availability is a significant service factor for frequent and occasional users, especially in developing countries (Tuan et al. 2022 ). Passengers anticipate a PT system that offers easy access without prolonged waiting times or difficulties reaching their desired destinations.

Another notable factor is crowdedness, which illustrates how a single SQ attribute can affect others. Crowdedness affects both comfort and safety on buses and can contribute to incidents of harassment against female passengers (Orozco-Fontalvo et al. 2019 ).

Challenges with first-mile and last-mile (hereinafter, FM/LM) connectivity are apparent, yet they are underexplored in the context of developing countries, necessitating further investigation. Other underexplored factors include connectivity (how well different modes of transportation are connected), transfers (the process of switching between various modes of transport), waiting environment (the conditions while waiting for transport) and waiting facilities (amenities provided for passengers while waiting). Climate change and heat stress can significantly impact the comfort and accessibility of PT in various ways. As temperatures rise due to climate change, extreme heat events become more frequent, posing challenges for passengers and the transport infrastructure. Rising temperatures due to climate change can lead to increased heat stress, especially during heatwaves, making waiting at outdoor transit stops uncomfortable and prolonged exposure to high temperatures while waiting for transit or during the journey can result in heat-related illnesses, affecting the well-being of passengers. Fraser and Chester ( 2017 ) posited that the design of transit systems, including the placement of stops and schedules, contributes to environmental exposure and may pose potential health risks, particularly during periods of extreme heat due to access and waiting. Improving the aesthetics of bus stops and incorporating diverse design elements can positively impact the thermal comfort of bus riders by enhancing their perception of beauty and pleasantness (Dzyuban et al. 2022 ). Addressing the effect of climate change on PT comfort and accessibility requires a comprehensive approach that involves collaboration between transit agencies, urban planners and policymakers. Sustainable and resilient solutions can increase the overall PT SQ in the face of changing climate conditions.

Until 2000, limited studies investigated SQ and commuters' satisfaction; since then, researchers focused primarily on qualitative assessments of the factors. The turning point for quantitative and qualitative assessments began in 2020 due to technological advancements that aided data collection procedures. As mentioned in Sect. 3 , there is a difference in how frequent and occasional users perceive SQ and their satisfaction. Further understanding of occasional users and improvements in these aspects can entice them to increase usage. In addition, the attitudes of private car users can provide valuable insights into their preferences, perceptions, and behaviours related to using PT systems.

4.2 Future research directions

Historically, transport researchers have explored the factors that influence PT usage. While our review uncovers valuable information, it also highlights significant areas that require further investigation. The first of these areas concerns exploring a less studied population group: private car users. Given the rise of private car acquisition and usage in developing countries, as mentioned in the introduction, shifting attention to this group is crucial. Recent attempts (Li et al. 2019a , b ; Al-Ayyash and Abou-Zeid 2019 ; Tao et al. 2019 ; De Magalhães and Rivera-Gonzalez 2021 ) have begun to address this, yet their approaches have been somewhat limited. For example, the target population for Al-Ayyash and Abou-Zeid ( 2019 ) included only university students and staff, which may not represent generalisability. Particular focus is required on SQ, satisfaction, and attitude towards PT. These areas are crucial for transport authorities and policymakers to intervene effectively.

The second area highlighted in the literature is problems with connectivity—FM/LM, but there is a paucity of literature. PT involves multiple journey stages, including waiting, walking, and switching between different modes, causing inconvenience (Park et al. 2021 ). The literature on transfers and satisfaction is scanty and conflicting. Das and Pandit ( 2015 ) noted more than two, Andaleeb et al. ( 2007 ) highlighted no transfers, and Li et al. ( 2020b ) indicated transfer convenience. Future studies must further probe transfers and their influence on PT usage and satisfaction. In addition, research should explore how transit authorities can adopt adaptive measures and sustainable practices to ensure that PT remains a reliable and comfortable option for all, even in the face of changing climate conditions.

Additional research avenue pertains to data collection methodologies. Qualitative research, such as interviewing individuals central to the subject, yields insights into PT usage factors. While most studies used questionnaires, there is potential for qualitative approaches. This approach aids in comprehending underlying influences by delving into the motivations behind mode shifts. For example, Mogaji and Nguyen ( 2021 ) investigated disabled commuters' satisfaction with PT using semi-structured interviews. Mystery shopping (MS) can also be employed for data collection. While MS in PT is known and implemented in practice, its exploration in academic literature remains limited, with only a few papers currently available (Voß et al. 2020 ). de Ona and de Ona ( 2015 ) and Voß et al. ( 2020 ) argued that using questionnaires in academic settings frequently lacks in-depth justification.

Finally, an area that may be explored is Mobility-as-a-Service (MaaS), which is gaining attention in developed countries and emphasising car access over ownership. Integrating bus transit within MaaS initiatives holds significant potential for enhancing urban mobility by providing users with seamless, multimodal transportation options. Several key factors influence the successful integration of bus transit into MaaS ecosystems, each playing a crucial role in shaping the accessibility, efficiency, and sustainability of PT networks.

Technology integration : One of the fundamental aspects of integrating bus transit into MaaS platforms is the seamless integration of technology. Users can conveniently access, plan, and pay for their bus journeys by leveraging mobile applications, contactless payment systems, and real-time tracking (Lyons et al. 2020 ). This technological integration enhances the overall user experience and encourages the adoption of bus transit as part of MaaS solutions.

Interoperability : Another critical factor is interoperability, which ensures the smooth integration of various transport modes within MaaS platforms. By enabling users to seamlessly switch between buses, trains, ridesharing, and micro-mobility services, interoperability enhances the flexibility and convenience of multimodal travel (Bushell et al. 2022 ). This interoperability requires collaboration between different transport providers and the development of common standards for data exchange and service integration.

Data sharing : Collaboration and data sharing among stakeholders are essential for optimizing bus transit services within MaaS ecosystems. By sharing data on routes, schedules, fares, and occupancy levels, transit agencies and technology providers can improve the efficiency and reliability of bus services (Chen and Acheampong 2023 ). Therefore, service integration is somewhat linked to the integration of data, which is indispensable for enabling service providers to make informed operational decisions (Kamargianni and Goulding 2018 ). This data-driven approach enables better planning, real-time monitoring, and predictive analytics, leading to more responsive and customer-centric transit operations.

Physical integration : This involves the physical infrastructure and connectivity between different modes of transport within a MaaS system, such as buses, trains, bikes, and ride-sharing services. Physical integration ensures seamless transfers and convenient access for passengers, enhancing the overall efficiency and attractiveness of the transit network (Saliara 2014 ).

Fare integration : It involves integrating fare payment systems across various modes of transport within a MaaS ecosystem. This allows passengers to use a single ticket or payment method to access different transit modes, including buses, trains, and ride-sharing services (Audouin 2019 ). Fare integration simplifies the passenger payment process, reduces transactional barriers, and encourages multimodal usage, ultimately enhancing public transport systems' overall efficiency and user experience.

Policy and regulation : Supportive policies and regulations play a crucial role in enabling the integration of bus transit into MaaS initiatives. Policies that promote open data standards, fare integration schemes, and public–private partnerships create an enabling environment for innovation and collaboration. Clear regulatory frameworks and support from central governments help address legal and governance issues and facilitate the implementation of MaaS solutions (Smith et al. 2018 ).

Partnerships and collaboration : Collaboration among public and private sector stakeholders is essential for driving innovation and fostering collective action towards integrating bus transit with MaaS initiatives. Partnerships between transit agencies, technology providers, urban planners, and community organisations enable the exchange of information, the consolidation of resources, and collaborative decision making (Merkert et al. 2020 ). Collaborative efforts contribute to developing integrated, user-centric MaaS solutions that address the diverse needs of urban populations.

4.3 Policy implications

The review offers a valuable understanding of the contemporary knowledge regarding the determinants influencing PT usage and the approach used to research them in developing countries. In this concluding section, we recommend enhancing the commuting experience and promoting greater utilisation of PT.

Identifying distinct SQ and satisfaction concerns while investigating ways to curb the rise in private vehicle usage can raise awareness among policymakers, transport operators, and transport authorities. Emphasising the alignment of SQ improvements with passengers' needs and expectations is crucial. This user-centric approach can foster more inclusive and customer-focused PT systems, as commuting experiences affect travellers' subjective well-being (De Vos et al. 2013 ). There are several instances where SQ improvements have an impact on ridership (with experiences also related to developed countries). For example, enhancements in comfort-related features of the Chicago transit system led to a notable 5% rise in the number of riders, equivalent to 15 million additional trips per year over 5 years (Foote 2004 ), enhancing the speed and frequency of buses in Ireland led to a decrease in car usage, reducing it from 34 to 22% (Redman et al. 2013 ), the introduction of an Integrated Ticketing System in cities such as London, New York, Haifa, Washington, Madrid, Chicago, various locations in Italy, San Francisco, Quebec, Montreal, and Seoul resulted in an increase in weekday patronage for both subway and bus services (Suman and Bolia 2019 ). SQ improvements are needed, and discourse on this subject requires attention.

In numerous developing countries, entrepreneurs primarily lead transport services, receiving limited governmental backing (Yeboah and Asibey 2019 ). Investments in transport infrastructure are necessary to curtail growing private car use for commuting. PT authorities should allocate resources towards sustainable modes of transport. For example, substantial investments in Australia's bus systems in recent decades have resulted in significant increases in ridership, primarily attributed to extensive service reorganisation and frequency improvements. Among these investments, BRT systems have demonstrated notable impacts at the corridor level, contributing to a 40% increase in new passengers from car drivers, a 17% increase from car passengers, and a 27% growth in new trips (Currie and Wallis 2008 ).

Data availability

Data sharing does not apply to this article as no datasets were generated or analysed during the current study.

Abbreviations

Automatic fare collection

Analysis of Variance

Automatic vehicle location

Cluster analysis

Confirmatory factor analysis

Customer satisfaction index analysis

Discrete choice experiment

Discriminant function analysis

Exploratory factor analysis

First-mile last-mile

Gradient boosting decision trees

Impact asymmetry analysis

Importance performance analysis

Importance-satisfaction analysis

Latent class cluster analysis

Level of Conformity

Multi-criteria decision making

Machine learning

Multinomial logit

Ordinal logit regression

Principal components analysis

Not available

Partial least squares

Penalty reward contrast analysis

Public transport

Random forest

Revealed preference

Structural equation modelling

Service quality (based on expectancy-disconfirmation paradigm)

Stated preference

Service quality

Urban transport passenger survey

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Acknowledgements

This manuscript is part of Eugene Sogbe's PhD research project. The authors sincerely thank Prof. Stefan Voß, the Editor-in-Chief, and two anonymous reviewers for their insightful feedback on the original manuscript. However, the authors acknowledge full responsibility for the contents of this paper.

Open Access funding enabled and organized by CAUL and its Member Institutions. This research was funded by Sunway Bhd. under the Scientific and technological approach to assessing the impact of elevated canopy walkways and bus rapid transit (BRT) on traffic in the Bandar Sunway project [Project ID: MRD-000006 and Grant code: 2600006-113-00].

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Department of Robotics and Mechatronics Engineering, School of Engineering, Monash University Malaysia, Jalan Lagoon Selatan, 47500, Bandar Sunway, Selangor, Malaysia

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E. Sogbe: conceptualization, methodology, formal analysis, writing—original draft, writing—review and editing, validation, resources, investigation, and visualization. S. Susilawati: supervision, writing—review and editing, project administration, and funding acquisition. C. P. Tan: supervision and data curation.

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Sogbe, E., Susilawati, S. & Pin, T.C. Scaling up public transport usage: a systematic literature review of service quality, satisfaction and attitude towards bus transport systems in developing countries. Public Transp (2024). https://doi.org/10.1007/s12469-024-00367-6

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Thermography, temperature, pressure force distribution and physical activity in diabetic foot: a systematic review.

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1. introduction.

The presence of diabetic neuropathy and its associated complications in the foot;
The magnitude of the forces exerted upon the foot;
The distance walked that results in the onset of tissue inflammation.

2. Materials and Methods

2.1. protocol and identification of the problem, 2.2. research question, 2.3. literature search strategy, 2.4. eligibility and selection criteria, 2.5. data collection, 2.6. assessment of study methodology and quality, 4. discussion, limitations and future research lines, 5. conclusions, author contributions, institutional review board statement, informed consent statement, data availability statement, conflicts of interest.

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Click here to enlarge figure

PICO Format
P (patient)	Healthy or diabetic subjects
I (intervention)	Measure plantar pressure and temperature and physical activity
C (control)	Healthy or diabetic patients
O (outcomes)	Changes in plantar temperature and pressure cause different plantar skin reactions during daily physical activity.

	Inclusion and Source	Random Assignment	Hidden Assignment	Baseline Comparability	Blinded Subjects	Blinded Therapists	Blinded Raters	Results above 85%	Analysis by “Intention to Treat”	Statiscal Comparisons between Groups	Measurement and Variability Data	Score
Di Benetto et al., 1996 [ ]	✓	✓	✓	✓	✓	✗	✓	✓	✓	✓	✓	9
Di Benedetto et al., 2002 [ ]	✓	✓	✓	✓	✓	✗	✓	✓	✓	✓	✓	9
Cuaderes et al., 2014 [ ]	✓	✗	✗	✓	✗	✗	✗	✓	✓	✓	✓	5
Maluf et al., 2001 [ ]	✓	✗	✗	✓	✗	✗	✗	✓	✓	✓	✓	5
Reddy et al., 2017 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Li et al., 2022 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Nemati et al., 2022 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Niemann et al., 2020 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Cabonell et al., 2019 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Yavuz et al., 2014 [ ]	✓	✓	✗	✓	✗	✗	✓	✓	✓	✓	✓	7
Priego Quesada et al., 2017 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
CataláVilaplana et al., 2023 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Perren et al., 2021 [ ]	✓	✓	✗	✓	✗	✗	✗	✓	✓	✓	✓	6
Jimenez et al., 2021 [ ]	✓	✗	✗	✓	✗	✗	✗	✓	✓	✓	✓	5

Author (Year)	Aim	Participants/Methodology	Intervention	Results
Di Benedetto et al. [ ] (1996)	To examine the regional effects of hypothermia in response to minor injuries.	A total of 1000 new male army recruits, aged between 17 and 21 years old, were divided into four groups. Group 1 comprised individuals with unilateral stress fractures and regional hypothermia, group 2 with unilateral stress fractures without regional hypothermia, group 3 with bilateral stress fractures without hypothermia and group 4 (controls) without musculoskeletal discomfort. AGEMA 870 thermographs were conducted.	Infrared imaging was conducted prior to and following the training period. In the event of pain and suspected stress fracture, a bone scan was conducted.	The sensitivity of the thermograms for detecting anomalies was high, but their specificity for basic diagnosis was low. It is possible that pain or injury to the lower extremities could cause an acute hypothermic response. However, hypothermia was not observed in recruits in the absence of significant pain. It can be hypothesised that therapeutic or self-imposed immobilisation could lead to hypothermia.
Di Benedetto et al. [ ] (2002)	Thermography should be employed as a diagnostic tool in cases of stress fractures that occur during military physical training.	New male army recruits aged 18 to 22 years, divided into three groups of 30 soldiers each. Group 1 (subjects with stress fractures), Group 2 (subjects with neuromuscular system problems but no fractures) and Group 3 (control subjects). AGEMA 870 thermographs were conducted using CATSE software.	Infrared images were obtained and plantar thermograms were analysed prior to the commencement of basic training, with subsequent assessments conducted whenever a subject exhibited neuromuscular or skeletal discomfort. In the event of suspected stress fracture, a bone scan was conducted.	The mean temperature was found to be 6 °C higher in cases of metatarsal stress fractures. The presence of hot spots was noted even in the absence of any discernible discomfort. Moreover, the aforementioned hot spots did not reappear in subsequent thermograms as the feet became acclimated to the novel stress. The incidence of stress fractures, particularly affecting the metatarsals, manifested in the third week as the intensity and duration of training increased. The aforementioned hot spots dissipated as the injuries underwent a process of healing. A correlation of 66% was observed between pain, bone scan results and the findings of thermograms. Soft tissue injuries manifested in regions exhibiting higher temperatures than those affected by bone injuries.
Cuaderes et al. [ ] (2014)	To assess diabetic sensory neuropathy and the plantar characteristics of pressure and temperature, among others, in adults after performing moderate-intensity weight-bearing activities.	A convenience sample of 148 individuals with diabetes was recruited for this study. Of these, 57 were athletes and 28 were non-athletes. The remaining 63 individuals were non-athletic and did not participate in sports. The gender distribution within each group was as follows: 57 female athletes, 36 male athletes, 27 female non-athletes, and 28 male non-athletes. The data set comprised measurements of plantar skin hardness (using a hand-held durometer), pressure in the sports shoes (scan in-shoe pressure) and plantar temperature (using an infrared dermal thermometer).	The volunteers were instructed to walk 30 paces at a self-selected pace. Following the completion of the test, data pertaining to temperature and plantar pressure were duly recorded.	The plantar pressure was observed to be higher in athletes, particularly women. The data indicated that the values were higher, particularly in the right midfoot locations (exercisers 1.79 ± 0.65; non-exercisers 1.61 ± 0.51, p = 0.03) and the region of the fourth and fifth toes of the left foot (exercisers 2.41 ± 1.51; non-exercisers 1.93 ± 1.13, p = 0.02). A comparison of the mean values for the two groups revealed that the left fourth metatarsal head exhibited a lower mean for the exercisers (2.64 ± 0.90) than for the non-exercisers (3.04 ± 1.47). A greater temperature gradient was observed in the plantar surface of the first metatarsal head in the athletes (exercisers 1.66 ± 1.31 and non-exercisers 1.20 ± 1.20, p = 0.02). The sole significant linear correlation between weight-bearing physical activity and plantar pressure was identified at the second metatarsal of the right head (r = 0.237, p = 0.02) and the third metatarsal of the head (r = 0.264, p = 0.01).
Maluf et al. [ ] (2001)	To validate a portable electronic device used to observe plantar pressures and temperatures, as well as the humidity of the foot inside shoes during prolonged activity.	Four healthy participants were equipped with shoe-mounted sensors to monitor pressure, humidity, and temperature. The data for pressure were collected in an uncontrolled outdoor environment, while the data for step count were gathered in an inner level walkaway and the data for humidity and temperature were obtained from a closed environmental control chamber.	The data were collected during a series of activities, including sitting down and rising from a chair, bending down to retrieve an object weighing 6 kg from a shelf at a height above the shoulders, traversing the stairs, walking on a level concrete surface, performing hip strategy walks and a pivot walk.	The combination of increased pressure, temperature and moisture inside the shoe could be a contributory factor in the development of plantar tissue injury. The inability of the researchers to identify individuals at risk of ulceration based on a predetermined pressure threshold may be attributed to the activity-related variations in foot pressure. It seems probable that the cumulative stress on the plantar tissues differed considerably between individuals, reflecting the variations in the quantity and nature of their daily activities. The environmental conditions within the shoe may influence the response of the plantar tissues to mechanical stress.
Reddy et al. [ ] (2017)	To examine the relationship between foot temperature and walking cadence and to determine how this affects the vertical pressures exerted on the foot.	Eighteen healthy volunteers were recruited for the study, divided into two age groups: one between 30 and 40 years old and the other over 40 years old. The insoles were constructed using canvas shoes (mod. 246,033 Slazenger) and incorporated temperature sensors (TMP35) in direct contact with the foot, along with a sock and pressure system (F-Scan, Model 3000E, Tek Scan Inc. Norwood, MA, USA).	Temperature, pressure and acceleration data were recorded with the patient sitting for 10 min, standing for 15 min, walking on a monitored treadmill (Ergo ELG 70, Woodway GmbH, Weil am Rhein, Germany) for 45 min and then sitting again for 20 min. Studies were performed at three different cadences (80, 100 and 120 steps/min).	Foot temperature increased by 5 °C during walking in both age groups and was greater with increased walking speed. Walking speed was found to be proportional to the increase in temperature, but the final temperatures recorded after walking did not differ. A maximum plateau value was observed, above which the foot temperature did not increase. There was an inversely proportional correlation between foot temperature during walking and before exercise, which was stronger in the older group. In both age groups, the increase in temperature did not correlate with the time integrals of the normal pressure exerted by the foot.
Li et al. [ ] (2022)	To examine the effects of shoe upper materials on foot relative humidity and temperature in older individuals. To examine the influence of the thermal environment of the footwear on the subjective sensation experienced while performing walking and sitting activities.	A total of 40 older individuals (25 female and 15 male) participated in the study, which involved walking and sitting in four different conditions: barefoot (Group A), wearing leather trainer shoes with an ethyl vinyl acetate sole (Group B), wearing mesh trainer shoes with an ethyl vinyl acetate sole (Group C) and wearing closed-toe trainer shoes with a rubber sole (Group D). An infrared camera (FLIR T420bx, Systems, Inc., Wilsonville, OR, USA) was employed to record skin temperature.	Following a 30 min period of foot conditioning while seated, the participants were required to complete two tests: a 20 min seated test and a 30 min treadmill walking test at a speed of 3 km/h. The mean recovery interval between the two tests was 15–30 min. Thermal images of the feet were obtained prior to and following each test. Three assessment scales were employed to measure thermal comfort and perceived humidity.	The temperature of the feet increased during the sitting position, with the greatest discrepancy observed between the barefoot condition (A) and the three shoe conditions (B, C, D, Y) on the dorsal aspect of the toes (2.8 °C, 1.2 °C and 1.8 °C, respectively) and on the heel (3.1 °C, 2.3 °C and 2.5 °C, respectively). In comparison to the barefoot condition, temperatures were observed to be higher for all shoe conditions during the walking phase of the trial. The highest temperature was recorded in group D. The greatest difference between the barefoot condition (A) and the three shoe conditions (B, C, Y D) was observed on the dorsal aspect of the toes, with a mean temperature of 2.3 °C, 1.4 °C and 2.4 °C, respectively. The temperature was higher for all shoe conditions at all regions of interest (ROIs) on the foot sole, with the exception of group C. The greatest difference in average temperature between groups A and B (2.4 °C) was observed in the toes. In comparison to the barefoot condition, groups C and D exhibited the most notable differences in the plantar arch, with a relative humidity increase of 2 °C and 2.5 °C, respectively. During the seated position, the greatest relative humidity increase was observed on the foot sole in shod conditions (B and D) and on the dorsal aspect of the foot in shod condition B. During ambulation, the relative humidity demonstrated a tendency to decrease with shoes, particularly in condition C, within the plantar arch. An increase was observed in the rear aspect of the foot in the B condition. Therefore, the degree of foot sweating was found to be greater in group B in comparison to groups C and D, both during periods of walking and sitting.
Nemati et al. [ ] (2022)	To develop a temperature-prediction model for the metatarsal area and plantar arch. To assess the precision of the model in forecasting the temperature of the foot sole.	Seven healthy adult males who were asked to wear running shoes without socks. The temperature of the feet was recorded at various points and at regular intervals using thermocouples.	Following a 10 min recovery period, participants engaged in a 30 min running exercise at speeds of 3, 6 and 9 km/h, respectively.	The maximum increase in plantar temperature was observed to be 6 °C, 8 °C and 11.5 °C for speeds of 3, 6 and 9 km/h, respectively. The cooling of the foot ‘by sweating’, as a thermoregulatory mechanism, was observed to be minimal at 3 km/h, with the first indications emerging after 15 min in the area of the plantar arch. At 9 km/h, this occurred after 20 min, while at 6 km/h, the onset was even later, occurring after 30 min. The role of sweating in the thermal regulation of the plantar arch was found to be fundamental, whereas in the metatarsal area, it was found to be insignificant.
Niemann et al. [ ] (2020)	To analyse the differences in plantar temperature changes during prolonged standing between healthy volunteers and diabetic patients with polyneuropathy.	A total of 31 healthy volunteers and 30 diabetic patients with polyneuropathy were included in the study. An insole equipped with eight pressure sensors (TTForce A01) and a temperature sensor (NTC 805) was developed for use in footwear worn by individuals with diabetes. Additionally, the temperature within the shoe was recorded without contact with the foot.	Pressure and temperature data were recorded during six episodes of standing, each lasting 5, 10 and 20 min, with a 5 min period of sitting between each episode.	The reduction in plantar temperature was significantly greater in the standing position compared to the seated position in both healthy and diabetic patients with polyneuropathy. However, the magnitude of the reduction in peak temperature did not differ between the two groups, reaching −1 °C for a period of 20 min and subsequently decreasing by a smaller magnitude throughout the remainder of the test. The healthy volunteers experienced discomfort in their feet during prolonged periods of standing, which necessitated brief episodes of pressure relief. This was not observed in patients with diabetes and polyneuropathy. A transient decrease in plantar temperature may precipitate injury during prolonged periods of standing.
Carbonell et al. [ ] (2019)	The objective is to evaluate the thermographic images in order to ascertain the effects of thermal and mechanical stress.	Thermal images of the feet of two groups of participants (15 diabetic patients and 7 healthy controls) were recorded with a termography camera (FLIR E-60, Flir Systems Inc., Wilsonville, OR, USA) at a distance of one metre. The ROIs were as follows: big toe, forefoot, midfoot and rearfoot.	Thermographic images were obtained prior to and following a 100 m treadmill walk, undertaken either barefoot or at a self-selected pace. Subsequently, a thermal stress (gel refrigerated at 0 °C) was applied to the soles of the feet, followed by thermographic video analysis of the basal thermal recovery rate over a 10 min period.	A greater reduction in temperature was observed in all ROIs in the diabetic patients following mechanical stress when compared to the control group. The greatest temperature differences between the groups were observed in the rearfoot and the forefoot, with a difference of −1 °C. The recovery of 90% of the basal temperature after thermal stress was observed to occur at a slower rate in diabetic patients.
Yavuz et al. [ ] (2014)	To analyse the relationship between plantar triaxial loading and post-excersice plantar temperature increase.	A total of 13 healthy volunteers participated in the study. An infrared camera (TiR2FT, Fluke Corporation, Everett, WA, USA) was utilised without the necessity for contact. A bespoke pressure shear plate had been constructed.	Participants walked on the shear plate at self-selected speeds using the two-steps method while the shear stress data were collected. Subsequently, the participants walked barefoot on a treadmill at a speed of 3.2 km/h for a period of 10 min, after which they returned to the shear plate to collect data pertaining to post-exercise shear stress. In the majority of cases, data from four trials were utilised. Temperature data were recorded at both the pre- and post-exercise stages.	The following variables were calculated: maximum shear stress (PSS), maximum resultant stress (PRS) and maximum temperature increase (AT). A moderate linear relationship was observed between PSS and AT. The post-exercise correlation between PSR and AT was found to be statistically significant (p = 0.002). Nevertheless, the location of the peak AT was unable to successfully predict the location of PSS in 23% of the volunteers. No statistically significant correlation was observed between AT and PRS. Moreover, in 39% of the subjects, the maximum temperature increase coincided with the peak observed in the study.
Priego Quesada et al. [ ] (2017)	To ascertain the relationship between the temperature of the sole of the foot (as determined by infrared thermography) and the occurrence of foot eversion during running (as observed through motion analysis).	A total of 22 runners (17 male and 5 female) completed a pre-test and a main test on different days, with a one-week interval between the two tests. The pre-test phase was conducted as follows: a maximal effort run of five minutes on a 400 m track was conducted to determine the maximal aerobic speed (MAS) of the subjects. The main test was conducted on a treadmill with an incline of 1% (Technogym SpA, Gambettola, Italy). The participants engaged in a 10 min warm-up at 60% of their maximal aerobic speed (MAS) before proceeding to run for 20 min at 80% of their MAS. The temperature of the feet was gauged with the aid of a thermal imaging camera (FLIR E-60, Flir Systems Inc., Wilsonville, OR, USA) prior to and following the test, while the occurrence of foot eversion was monitored throughout the test. ROIs were defined as follows: the rearfoot (with a defining length of 31% of the entire plantar surface of the foot) and the medial and lateral ROIs (defined as 50% of the maximum foot width).	Thermal images were obtained from each participant at three distinct time points: prior to, immediately following and 10 min following the completion of the running test. During the running test, the participants were barefoot, wearing only their running shoes.	A weak negative correlation was observed between contact-time eversion values and rearfoot thermal symmetry immediately following the running session, while a weak positive correlation was evident between these variables and rearfoot thermal asymmetry at the final temperature. The maximum eversion values exhibited during the stance phase demonstrated a weak negative correlation with foot thermal symmetry, as assessed immediately following the running session, and a weak positive correlation with foot thermal asymmetry at the final temperature.
Catalá-Vilaplana et al. [ ] (2023)	To analyse the impact of different types of sports footwear (traditional stable shoes vs. unstable shoes) on acceleration impacts on the tibia and forehead, as well as the variation in plantar surface temperature.	Six athletes (four female and two male) were assessed on two separate occasions, with a one-week interval between each assessment. On the initial assessment day, anthropometric variables (height and body weight) were recorded, and the foot typology was characterised using the Foot Posture Index. On the second day, the treadmill walking test was conducted under two footwear conditions: stable shoes (Adidas Galaxy Elite Noir) and unstable shoes (Skechers Shape Ups). Two triaxial accelerometers with a frequency of 420 Hz were used, one on the distal tibia of the dominant leg and another on the forehead (MMA7261QT, Free-scale Semiconductor©, Munich, Germany). The surface temperature of the feet’s soles was determined through the utilisation of a thermal imaging camera (FLIR E60bx, Wilsonville, OR, USA). The ROIs were evaluated for each of the three anatomical areas: the forefoot, midfoot and rearfoot.	The participants walked for a period of ten minutes with each type of footwear at a speed of 1.44 metres per second, with a two-hour period of rest between each test. The spatiotemporal and acceleration variables were obtained from the three eight-second recordings taken at minutes 2, 5 and 9 of each test. Thermal records were obtained at three distinct time points: prior to the test, immediately following the test and five minutes after the conclusion of the test.	No statistically significant differences were identified in any of the accelerometry variables. Significant differences were observed in the thermographic images between the pretest and post-five time points, particularly in the midfoot region (p = 0.004, ES = 1.2).
Perren et al. [ ] (2021)	To determine whether there was a correlation between pressure and temperature in different regions of the foot across different categories of participants after a 15 min walk.	The study population comprised four groups of 12 individuals (a total of 42 males and 6 females), as follows: healthy patients (Group A), patients with diabetes (Group B), diabetics with peripheral arterial disease (Group C) and diabetics with neuropathy (Group D). A Tekscan high-resolution (HR) treadmill (Tekscan, Boston, MA, USA) was utilised to collect plantar pressure data. The following ROIs were evaluated: the hallux, the first metatarsophalangeal joint (MPJ), the second to fourth MPJs, the fifth MPJ and the heel. Thermal imaging was conducted using a thermal camera (T630C FLIR, Wilsonville, OR, USA).	The results of three pressure tests were recorded for each participant while they were walking at their preferred speed. Subsequently, the participants were positioned in a supine position on the examination table for a period of 15 min. Subsequently, the participants were required to walk for a period of fifteen minutes on a treadmill. One minute after cessation of ambulation, thermograms were obtained of the plantar surface of the feet.	In the preliminary statistical analysis, the four groups were consolidated into two categories: a control cohort comprising groups A and B and a complication cohort comprising groups C and D. In the groups exhibiting complications, a positive correlation was observed between temperature and pressure in the hallux and the second to fifth metatarsophalangeal joints (MPJs) as well as in the heel ROIs. This correlation was exclusive to the fifth metatarsophalangeal joint in the healthy cohort. In the second statistical test, the two groups were divided into a healthy cohort (Group A) and a diabetes cohort (Groups B, C and D). A positive correlation was observed between temperature and pressure for all ROIs in the diabetes group, whereas in the healthy group, this correlation was evident only for the 2nd–5th MPJs. In individuals without complications (groups A and B), there was a tendency for pressure areas to become warmer, although this was less significant than in individuals with complications (groups C and D).
Jiménez et al. [ ] (2021)	To establish a correlation between plantar pressures during prolonged running and plantar temperature, whether in the sole of the foot or the sole of the shoe.	A total of 30 recreational runners (15 males and 15 females) were recruited to perform a 30 min running test on a treadmill (Excite Run 900, Technogym Spa, Gambetta, Italy). Thermographic images were obtained of the sole of the feet and the sole of the shoes using an infrared camera (Flir E60bx, Flir Systems Inc., Wilsonville, OR, USA) at two time points: immediately prior to the commencement of the test and at its conclusion. Subsequently, dynamic plantar pressure was quantified at 200 Hz using an F-Scan in-shoe pressure measurement system (v.50, Tekscan Inc., Boston, MA, USA).	The participants engaged in a six-minute treadmill running session, which was followed by a 30 min treadmill running session with a 1% slope. This was done in order to simulate the duration and intensity of regular training. Two thermographic images were obtained of the soles of the dominant feet and the soles of the sports shoes in a seated position. The initial image was captured one minute prior to the commencement of the 30 min trial, with the subsequent image obtained one minute thereafter. At the conclusion of the trial, dynamic plantar pressure was assessed.	A moderate correlation was observed between plantar pressure and plantar temperature, both in the soles of the feet and in the soles of the shoes, particularly in the forefoot regions. The correlation between plantar pressure and plantar temperature was more pronounced in the shoe soles than in the foot soles. Following the running exercise, the temperature of the shoe soles was observed to be lower in the female participants than in the male participants.

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Rosell-Diago, M.P.; Izquierdo-Renau, M.; Julian-Rochina, I.; Arrébola, M.; Miralles, M. Thermography, Temperature, Pressure Force Distribution and Physical Activity in Diabetic Foot: A Systematic Review. Appl. Sci. 2024 , 14 , 8726. https://doi.org/10.3390/app14198726

Rosell-Diago MP, Izquierdo-Renau M, Julian-Rochina I, Arrébola M, Miralles M. Thermography, Temperature, Pressure Force Distribution and Physical Activity in Diabetic Foot: A Systematic Review. Applied Sciences . 2024; 14(19):8726. https://doi.org/10.3390/app14198726

Rosell-Diago, Maria P., Marta Izquierdo-Renau, Iván Julian-Rochina, Manel Arrébola, and Manuel Miralles. 2024. "Thermography, Temperature, Pressure Force Distribution and Physical Activity in Diabetic Foot: A Systematic Review" Applied Sciences 14, no. 19: 8726. https://doi.org/10.3390/app14198726

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AI Tools for Systematic Literature Reviews

Sep 25, 2024 | News and Trends

Polly Field , Tomas Rees and Richard White , Oxford PharmaGenesis, UK

Email your questions and comments on this article to [email protected] .

A systematic literature review (SLR) allows us to find and evaluate existing evidence to answer a specific research question. But with increasing interest in reviews that are rapidly updated and cover a wide evidence-base – an evidence base that is increasing with the exponential growth in the volume of scientific literature – we see increasing demands on the resources needed to develop these reviews, with multiple people required to ensure that the methods are reproducible, and the evidence is accurate. This is one reason that many people are turning to artificial intelligence (AI), especially when considering large and complex SLRs, which would otherwise not be feasible without AI because of cost or turnaround time.

Here we consider how and when AI should be used to develop SLRs for publication, drawing on our experience as AI users, SLR experts and publication professionals. We provide guidance on the potential applications of AI, and the issues that should be considered when choosing an AI-based approach, deliberately avoiding describing specific tools, as these are evolving daily.

What advantages can AI bring?

AI can help with the scale, efficiency, quality and understanding of some SLRs.

Scale/volume of evidence: AI can enable literature reviews at scales not previously considered feasible. The larger the SLR, the greater the benefit.
Efficiency: AI can learn from initial work, speeding up subsequent updates, for example by using LLM screening questions (prompts) optimized in the initial review or by fine-tuning ML algorithms on the original data set.
Quality: use of AI, with appropriate checks, has the potential to improve accuracy and reduce researcher bias.
Understanding: AI can help summarize, group and visualize data, revealing patterns and trends in the underlying information.

How can AI help in the different stages of an SLR for publication?

AI can help across the full workflow of SLR development if used correctly and with people to check and adjust the output. 2 In Figure 1, we describe current major uses by stage, deliberately not describing specific tools.

Considerations for evaluating AI tools for use in SLRs for publication

Before using a tool or platform, it should be critically appraised to understand potential advantages and risks. This includes testing of usability – whether the team can easily interact with the AI and incorporate it into the SLR workflow – and testing of performance, including sensitivity, specificity, time and resource use. There are important ethical, practical, business and legal considerations when using AI relating to the following risks.

Any data, information or files uploaded into an AI tool may essentially become public domain or be used to train a provider’s AI model, potentially breaching confidentiality and/or copyright. Choice of provider and careful assessment of how they use any data uploaded to the tool is key.
LLMs are trained on massive data sets of existing text. By analyzing these data, the AI learns the patterns and relationships within that content, which, following more training, gives them the ability to perform specific tasks like answering questions about a document. AI does not understand what it is creating and cannot judge the quality, usefulness or correctness of what it generates.
In general use, LLMs tend to adhere to text patterns that occur in their training set. They can easily generate material that is grammatically correct and convincingly written, but factually or logically incorrect. In the SLR context, this is mitigated by using retrieval-augmented generation, in which contextual content is provided to the LLM for use in developing the output. Many tools enable the user to easily validate LLM responses by highlighting the source text. This helps with fact-checking, but errors of omission remain a challenge.

Fundamental principles for the use of AI in SLRs for publication

The use of AI in any project should be aligned with relevant formal institutional and corporate policies for all parties involved, assuring a consistent and ethical approach. A fundamental principle of any publication is that the authors of an SLR are responsible for the quality and accuracy of their work, whether developed entirely by themselves or with assistance from AI; the use of AI does not alter the authors’ ownership of quality.

Explainability and reproducibility – these are key challenges with SLRs, even when conducted by humans. LLMs add to the problem because they are by nature stochastic. Furthermore, differences in training sets and decisions in model development are often not adequately disclosed by the developers (this affects some tools more than others).
Appropriateness of AI to the question being asked and the available evidence – the potential benefits of using AI in the various stages of the SLR process will differ with every project. For example, a novel therapeutic modality being used in a previously untreatable rare disease may have a small corpus of literature utilizing a broad range of terminology and new endpoints, which will be challenges for the use of existing LLMs or training of new ML approaches.
Transparency in the use of AI and its reporting – everyone involved in an SLR should agree to the use of AI, and the approaches taken should be clearly described in subsequent publications in line with relevant journal or conference guidelines.
Assuring quality and accuracy – humans providing expert knowledge and oversight are crucial; AI should be considered an augmentation, not a human replacement. A rigorous methodology with multiple layers of human validation should be developed and agreed by all authors involved in the SLR, noting that reviewing AI-generated material requires not just more checking, but a different focus while checking.

What guidelines exist for the use of AI in SLRs for publication?

The use of AI is captured in many guidelines related to publication and SLR methodology, and it is important to ensure compliance. The International Committee of Medical Journal Editors recommendations note that authors using AI to conduct a study (which we take to include AI use in literature reviews) should describe its use in the methods section in sufficient detail to enable replication of the approach. 3 It further notes that authors using AI for writing assistance should report this in the acknowledgments section. 3 Many journals also have policies about the use of generative AI, and authors should check the policy of the specific journal ahead of submitting a review to ensure compliance. Overall, policies accept that authors can use generative AI, providing that they maintain responsibility for the content and accuracy of the work. This can mean that AI is used to help with exploring ideas, searching and classifying literature, and improving the language used, but that authors are accountable for the originality, validity and integrity of their work. The Preferred Reporting Items for Systematic Reviews and Meta-Analyses guidelines are widely used for the reporting of SLRs, and the 2020 statement includes guidance on how the use of AI should be reported. 4 This is limited to the early stage of the review, with authors asked to report the number of records that are removed before screening. 4

Conclusions

AI is here to stay and can help medical publication professionals develop high-quality work, including SLRs for publication. It is up to all of us to keep engaging, to be alert to new approaches and applications, and to evaluate, upskill and start to use these new and evolving tools. Above all, we need to stay transparent and acknowledge our use of AI, making clear that humans remain responsible for the quality of SLRs.

Acknowledgments

This article was critically reviewed by Kim Wager, Martin Callaghan, Gemma Carter and Jacob Willet from Oxford PharmaGenesis; Jody Filkowski from Medlior contributed to the original planning and content of the article.

Bibliography

Higgins JPT, Thomas J, Chandler J et al. Cochrane Handbook for Systematic Reviews of Interventions version 6.4 (updated August 2023). Cochrane, 2023. Available from www.training.cochrane.org/handbook .
Teperikidis E, Boulmpou A, Potoupni V et al. Does the long-term administration of proton pump inhibitors increase the risk of adverse cardiovascular outcomes? A ChatGPT powered umbrella review. Acta Cardiol 2023;78:980–8.
International Committee of Medical Journal Editors. Recommendations for the Conduct, Reporting, Editing, and Publication of Scholarly Work in Medical Journals (updated January 2024). Available from https://www.icmje.org/news-and-editorials/icmje-recommendations_annotated_jan24.pdf (Accessed 12 August 2024).
Page MJ, McKenzie JE, Bossuyt PM et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. Syst Rev 2021;10:89.

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Item 4. Online resources and browsing

Web search engines and specific web sites

Conference proceedings

General browsing

Item 5. Citation searching

Item 6. Contacts

Item 7. Other methods

Item 8. Full search strategies

Item 9: Limits and restrictions

Item 10. Search filters

Item 11. Prior work

Item 12. Updates

Item 13. Dates of searches

Item 14. Peer review

Item 15. Total records

Item 16. Deduplication

Part 5. Discussion and conclusions

Availability of data and materials

Abbreviations

Acknowledgements

Author information

Contributions

Corresponding author

Ethics declarations

Consent for publication

Competing interests

Additional information

Supplementary Information

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Methodology

Author summary

Introduction

Literature search

Inclusion and exclusion criteria

Data extraction

Statistical analysis

Meta-analysis

Study characteristics

Diagnostic methods

Prevalence distribution

Serovar and species distribution

Clinical signs and symptoms