https://orcid.org/0000-0002-9284-6630
Figures
Abstract
Background
Sexually Transmitted Infections, including Neisseria gonorrhoeae (NG) and Chlamydia trachomatis (CT), continue to be a global health problem. Increased access to point-of-care-tests (POCTs) could help detect infection and lead to appropriate management of cases and contacts, reducing transmission and development of reproductive health sequelae. Yet diagnostics with good clinical effectiveness evidence can fail to be implemented into routine care. Here we assess values beyond clinical effectiveness for molecular CT/NG POCTs implemented across diverse routine practice settings.
Methods
We conducted a systematic review of peer-reviewed primary research and conference abstract publications in Medline and Embase reporting on molecular CT/NG POCT implementation in routine clinical practice until 16th February 2021. Results were extracted into EndNote software and initially screened by title and abstract by one author according to the inclusion and exclusion criteria. Articles that met the criteria, or were unclear, were included for full-text assessment by all authors. Results were synthesised to assess the tests against guidance criteria and develop a CT/NG POCT value proposition for multiple stakeholders and settings.
Findings
The systematic review search returned 440 articles; 28 were included overall. The Cepheid CT/NG GeneXpert was the only molecular CT/NG POCT implemented and evaluated in routine practice. It did not fulfil all test guidance criteria, however, studies of test implementation showed multiple values for test use across various healthcare settings and locations. Our value proposition highlights that the majority of values are setting-specific. Sexual health services and outreach services have the least overlap, with General Practice and other non-sexual health specialist services serving as a “bridge” between the two.
Citation: Fuller SS, Clarke E, Harding-Esch EM (2021) Molecular chlamydia and gonorrhoea point of care tests implemented into routine practice: Systematic review and value proposition development. PLoS ONE 16(11): e0259593. https://doi.org/10.1371/journal.pone.0259593
Editor: Catherine E. Oldenburg, University of California, UNITED STATES
Received: July 28, 2021; Accepted: October 21, 2021; Published: November 8, 2021
Copyright: © 2021 Fuller 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 relevant data are within the manuscript and its Supporting information files.
Funding: The authors received no specific funding for this work.
Competing interests: We have read the journal’s policy and the authors of this manuscript have the following competing interests: ADREU has received funding from Abbott, binx health, Cepheid, SpeedDx, Mologic, Revolugen and Sekisui, for the research and evaluation of their diagnostics. SSF was a co-investigator on Innovate UK grant to binx health, "A stratified medicine diagnostic test for STI patients at the point-of-care" (ref: 971543) and is a consultant for the WHO on point-of-care tests for sexually transmitted infections. EHE and EC report that no competing interests exist. This does not alter our adherence to PLOS ONE policies on sharing data and materials.
Abbreviations: CE, Conformité Européene; CT, Chlamydia trachomatis; ED, Emergency Department; FDA, Food and Drug Administration; GP, General Practice; GPS, Global Positioning System; LMICs, Low- and Middle-Income Countries; NG, Neisseria gonorrhoeae; POCT, Point-of-Care-Test; STI, Sexually Transmitted Infection; TPP, Target Product Profile; TV, Trichomonas vaginalis; WHO, World Health Organization
Introduction
It is estimated that there are over 1 million new curable sexually transmitted infections (STI) cases every day; in 2016 there were approximately 376 million new cases of the most common curable STIs: Neisseria gonorrhoeae (NG), Chlamydia trachomatis (CT) Trichomonas vaginalis (TV), and syphilis [1]. If left untreated, these infections can result in serious reproductive health sequelae, such as infertility, chronic pelvic pain, ectopic pregnancy, and pelvic inflammatory disease. CT and NG infections are two key STIs: CT is the most commonly reported STI [2], and treatment of NG is a global public health problem following the emergence of multi-drug resistant strains [3].
Syndromic management (diagnosis and treatment of STIs based on patients’ clinical history and reported and observed symptoms) has been shown to be both poorly sensitive and specific for STI diagnosis [4]. It can result in asymptomatic but infected individuals not being treated, resulting in continued transmission and development of reproductive health sequelae. Conversely, symptomatic patients of unknown aetiology may receive unnecessary, inappropriate and/or sub-optimal treatment, potentially increasing the risk of STI antimicrobial resistance (AMR) emergence [5]. STI diagnosis is therefore ideally informed by diagnostic tests, and there has been a marked move away from syndromic management, wherever possible, in the majority of high-income settings [6]. However, in LMICs, syndromic management is still commonplace. There is little access to large-scale laboratories, as well as a lack of highly skilled healthcare professionals and specialised equipment in clinical settings, which are needed for aetiological diagnosis of STIs [4, 5].
Diagnostics have been hailed as a critical intervention to reduce the global burden of AMR [3], with a growing need for the development of point-of-care tests (POCTs) to combat the global STI health burden [6, 7]. The World Health Organization (WHO) defines POCTs as those that can be used at, or near, the point of patient care [8]. Guidelines and criteria for optimal diagnostics have been published to both guide test development and assess their ability to meet STI control requirements in all settings [9–12]. These include the REASSURED criteria (Affordable, Sensitive, Specific, User‐friendly, Rapid and robust, Equipment‐free and Deliverable to end‐users, recently updated to also include advances in m-health, incorporating both “Real-time connectivity” and “Ease of specimen collection”) [9, 11]. These criteria focus on the needs of LMICs and were developed by WHO’s STD Diagnostics Initiative as a benchmark to determine whether POCTs for community level (level 1 health centres) use meet local requirements for STI prevention, control and management [13]. Furthermore, POCT Target Product Profiles (TPPs) for specific infections have been created by WHO through consultation with experts. These TPPs focus both on LMIC and higher-income country needs, and include multiple minimal and optimal characteristics, from diagnostic accuracy characteristics to cost [12]. TPPs aim to help accelerate and guide future STI POCT development [12].
There are various POCTs for CT and NG diagnosis available [8, 14, 15]. Non-molecular testing for NG includes Gram stain microscopy, which requires specialist equipment and a high-level of training of healthcare professionals within the clinic [16]. For CT, commercial antigen detection lateral flow tests have been developed with the ASSURED criteria in mind: they are low-cost, equipment-free and easy to perform, but offer suboptimal sensitivity for diagnosis [12, 17]. International guidelines stipulate that diagnosis of CT and NG should be based on results from highly-accurate molecular tests wherever possible [18–21]. To date, two highly accurate molecular POCTs for CT and NG have obtained Conformité Européene (CE) marking from the European Union, and United States Food and Drug Association (FDA) regulatory approval, both of which offer CT/NG dual detection: the Cepheid GeneXpert, with a 90-minute time-to-results [22], and the binx health io with a 30-minute time-to-results [23].
However, even diagnostics with excellent clinical trial outcomes face multiple barriers to adoption [24, 25]. Although TPP and REASSURED criteria are useful frameworks for test development and evaluation, different values for adoption, such as clinical, process and financial outcomes, are negotiated during implementation [26]. It is increasingly recognised that the social and structural context of implementing a new technology is as important as evidence for its clinical effectiveness [27–29], and that these should be reviewed from the different perspectives of multiple stakeholders [24, 30, 31]. Stakeholders are defined as any person or organisation contributing to a care pathway, including patients, carers, healthcare professionals, provider organisations, purchasers of healthcare services, policymakers and laboratory medicine specialists [32].
The value of POCTs is likely to differ both within and between different stakeholder groups, who often have varying priorities and objectives [33]. It is important to understand these values to facilitate the integration of POCTs into sexual healthcare. There are many proposed frameworks to measure value [34], one of which is the value proposition of laboratory medicine [35]. It aims to facilitate the implementation of innovations in healthcare by consolidating and making visible the available evidence of the innovations’ costs and benefits to different stakeholders [35]. It also considers values beyond clinical trial data, arguing that in an outcomes-based health system, the value of an innovation to all stakeholders must be measured and communicated [32, 35, 36].
We aimed to develop a value proposition for molecular CT/NG POCTs that is reflective of the needs of different sexual healthcare stakeholders, in order to facilitate decision-making processes for implementation and adoption of CT/NG POCTs into diverse care settings.
Methods
The overall research question was: “What are the outcomes of molecular CT/NG POCTs implementation for patients being tested for CT/NG in different routine practice settings?” To answer this question, we developed three specific objectives: i.) What values are placed on CT/NG POCTs implemented in routine practice in the published literature? ii.) Do molecular CT/NG POCTs implemented in routine practice fulfil the (RE)ASSURED and TPP criteria? iii.) What is the value proposition for molecular CT/NG POCTs by setting, based on the value proposition for laboratory medicine [35]?
To meet our first objective, we conducted a systematic review of the published literature reporting on molecular CT/NG POCT implementation in routine clinical care. To meet the second objective, we reviewed and assessed compliance of the tests identified through the systematic review to REASSURED and TTP criteria for STI POCT development, using data from formal diagnostic evaluations. For the third objective, we developed a CT/NG POCT value proposition based on a synthesis of the wider available evidence. Data from additional studies evaluating NAAT-based test(s) for CT/NG, but that were ineligible for the systematic review (e.g. research-only outcome, such as diagnostic accuracy studies; or not primary research, such as cost-effectiveness modelling), were extracted. These were applied to the value proposition for laboratory medicine framework [35] to develop a value proposition for molecular CT/NG POCTs, by setting type. Data were tabulated to meet each objective, and a narrative synthesis of results (i.e., rather than a metanalysis) was conducted by SSF and EMHE, given the heterogeneity of study designs and settings.
The systematic review was conducted in MEDLINE and Embase (OvidSP interfaces) to include all peer-reviewed primary research and conference abstract publications until 16th February 2021 (S1 and S2 Tables). Both MEDLINE and Embase (OvidSP interfaces) were searched by one researcher (EC) for studies involving human participants using a combination of terms and synonyms based on four key concepts (chlamydia AND gonorrhoea AND point of care tests AND evaluation). For full details of search terms please see S1 Table. We report our review following the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) guidelines [37] (S2 Table).
Results were extracted into EndNote (Clarivate Analytics, Philadelphia, USA), and duplicates removed. Titles and abstracts were screened by EC according to the inclusion and exclusion criteria (Table 1). Articles that met the criteria, or any that were unclear, were included for full text review by all authors independently, with any discrepancies discussed as a group to reach consensus for final inclusion. SSF and EMHE independently extracted data from eligible articles into custom-made Excel (v2019, Microsoft) tables. References of included papers were also hand-searched by EC and new potentially eligible articles full-text screened by all authors before confirming inclusion, with data independently extracted by SSF and EMHE.
Study quality was assessed by SSF and EMHE, independently, using the Critical Appraisal tools for use in JBI Systematic Reviews where possible ([38] as recommended by [39]; S3–S7 Tables). For studies where the CT/NG POCT was implemented as routine (e.g. service evaluations), we modified the JBI checklist for analytical cross-sectional studies by removing the three questions relating to exposure and confounding, as no JBI checklists were appropriate. For before-after studies, the NHLBI quality assessment tool was used [40]. For questionnaire-based studies, the Center for Evidence-Based Management “Critical appraisal of a survey” checklist was used ([41] as recommended by [42]). Any differences between the two reviewers were reconciled through discussion to provide an overall study quality score calculated as number of questions with a “yes” response divided by the total number of questions. Any questions that were non-applicable were removed from the denominator.
We did not produce a protocol or register this study.
Results
The systematic review search returned 440 articles, of which 26 were included for review. After the references of the 26 included articles were checked to confirm completeness, two further articles were eligible, which led to a final inclusion of 28 articles (Fig 1). Study quality assessment indicated that 5 studies were of low quality (≤50% criteria met), 4 studies were of medium quality (between 50 and 75% of criteria met) and the remaining 19 articles were of high quality (≥75% criteria met) (S3–S9 Tables).
From: Page MJ, McKenzie JE, Bossuyt PM, Boutron I, Hoffmann TC, Mulrow CD, et al. The PRISMA 2020 statement: an updated guideline for reporting systematic reviews. BMJ 2021;372:n71. doi: 10.1136/bmj.n71. For more information, visit: http://www.prisma-statement.org/.
The binx health io CT/NG has been implemented in a small number of clinical settings, however, available reports show the test being implemented in research-use only scenarios in the USA [43, 44] and publications (to-date of this review) reporting implementation in the UK do not report clinical and other health-related outcomes [45]. The Cepheid CT/NG GeneXpert has been implemented and evaluated for multiple outcomes measures in many settings around the world. As such, only the Cepheid GeneXpert platform, using the CT/NG dual diagnostic cartridge, was eligible for assessing compliance with international guidelines for CT/NG POCT development and evaluation, and evaluating the values placed on CT/NG POCTs implemented in routine practice in the published literature.
TPP and REASSURED criteria provide checklists to guide the development and evaluation of STI POCTs. A summary of both these frameworks for CT/NG POCTs is presented below (Table 2); these reflect a summary of published evaluations of the Cepheid CT/NG GeneXpert diagnostic performance.
TPP recommendations for CT/NG POCTs
WHO TPP recommendations for CT/NG POCTs include: sensitivity (NG: 90% minimal, 98% optimal; CT: 90% minimal, 100% optimal) and specificity (NG and CT: 98% minimal, 100% optimal); training requirements (<90 minutes minimal, <30 minutes optimal); time-to-results (<60 minutes minimal, <30 minutes optimal) and price per test (<5 USD minimal, <1 USD optimal) [12]. Other considerations include the inclusion of a Global Positioning System (GPS) on the platform reader, and sample capacity/through-put [12]. Operational use prioritisation is suggested to be in the following order: ease of use, training, high tolerance to difficult environmental conditions and long shelf life, self-contained quality control, data capture/connectivity/data export, biosafety and waste disposal [12].
REASSURED criteria
The REASSURED criteria are: Real-time connectivity (feedback for patient treatment and connection to surveillance systems); Ease of specimen collection and Environmentally-friendly (non-invasive specimen collection; use of recyclable materials and reduction of hazardous waste); Affordable (<10.00 USD for a molecular assay); Sensitive (minimising false negatives) and Specific (minimising false positives); User-friendly (2–3 steps and minimal training required); Rapid and robust (15–60 minutes from sample-in to answer-out; withstands various weather and environmental conditions without refrigeration); Equipment-free (or utilises batteries or solar power) and Deliverable to end-users (ensures it reaches LMIC users) [11].
Published diagnostic evaluations show that the Cepheid CT/NG GeneXpert fulfils some, but not all, TPP and REASSURED criteria (Table 2). Minimal sensitivity and specificity requirements are met for genital samples, but not for extra-genital samples for CT. Training may be considered too long at “less than half a day”, compared with the minimal TPP requirement for <90 minutes. The 90-minute time-to-results is longer than the 60-minute minimum of both criteria frameworks, and the cost is higher than the 10 USD recommendation for the REASSURED criteria. In addition, the test is not environmentally friendly, as it uses a single-use cartridge to be disposed of via local medical waste regulations. However, the test can be used with non-invasive specimen types, does feature connectivity for monitoring, surveillance and data export, and is user-friendly with automated sample preparation and a three-step process from sample provision to processing. It also features a sample adequacy control for internal quality control purposes. The REASSURED criteria “deliverable to end-users” can be considered contextually, such as the tests’ compatibility with diagnostics currently in use (e.g. current use of the GeneXpert platform for tuberculosis or TV testing [46]), which relate to potentials to use pre-existing procurement and test supply chains in those settings.
Data from eligible articles were extracted to show the value of implementing the Cepheid CT/NG GeneXpert in three different healthcare service settings (specialist sexual health services, General Practice [GP] and other non-sexual health specialist services, and outreach services), spanning different income settings (Table 3).
Implementation of the Cepheid CT/NG GeneXpert demonstrated that faster (and appropriate) treatment was achieved in all settings. This was facilitated by reduced time to notification of results, which was a specific outcome for some studies [47, 58, 60, 63, 69] but same-day treatment was hindered by patients not waiting for test results at the point of care [61, 65], and one study specifically reported increased patient waiting time in-clinic [57]. However, implementation of the test was broadly acceptable in all settings reporting this as an outcome [55, 61, 66–68, 72]. In non-sexual health services, introduction of the Cepheid CT/NG GeneXpert enabled detection of STIs, a service which previously had not been available [57, 64, 66, 67, 69]. Additional benefits beyond immediate patient management were also recorded, including improving partner treatment, reducing transmission, and cost-savings [47, 55, 65, 69].
In Table 4, in addition to the Cepheid CT/NG GeneXpert studies included in Table 3, we report on a wider literature of stakeholder values for implementation of POCTs, including reports of the binx health io CT/NG. Studies reporting implementation of the binx CT/NG in a sexual health specialist service and a University student health clinic (outreach service) in the USA were restricted to implementation without results delivery; at the time of the studies the test was not yet FDA approved [43, 44, 73]. Publication of a UK-based project tracing implementation into routine care did not include assessment of clinical outcomes [73]. Nevertheless, the available studies (albeit limited to the USA and UK) have shown implementation processes of this CT/NG POCT to be highly acceptable to patients [43, 44] and healthcare workers [44, 45, 73].
Some of the values for molecular CT/NG POCTs cross-cut all settings: unmet need, care pathway context, and accountability. However, the majority of values are setting specific. Sexual health services and outreach services have the least overlap in values, whereas GP and other non-sexual health specialist services “bridge” between them. GP and other non-sexual health specialist services and outreach services share the value that the test is most likely to be used as a screening tool to increase testing, rather than the multiple purposes of screening, diagnosis, and guiding use of treatment, as is necessary in sexual health services. Non-specialist settings also have similarities for evidence of cost-effectiveness and translation challenges as this often requires new staff and training [52, 74, 75]. Sexual health services and GP and other non-specialist services overlap most for change in practice and change in resource requirement, and implementation metrics.
Discussion
The Cepheid CT/NG GeneXpert test was the only molecular CT/NG POCT to have been implemented and evaluated as part of routine practice in the published literature. Although it did not meet all TPP or REASSURED criteria, review of its implementation and reported benefits demonstrated this did not preclude it from bringing value to a service or its stakeholders. Of note, although the cost-per-test of the Cepheid CT/NG GeneXpert exceeds the minimum TPP and REASSURED recommendations [49], cost-effectiveness models show relative value-for-money of POCTs when considering onward transmission and progression of disease [50, 75–78]. Thus, it is only when these tools and frameworks are examined within the delivery context that sense-making happens around the adoption and implementation decision-making processes [26, 79]. This was further emphasised when extracting these findings for development of the value proposition, where we found that values differed both within and between healthcare settings.
To our knowledge, this is the first report that systematically reviews the literature on molecular CT/NG POCTs’ implementation in routine practice, to assess the value different stakeholders in different settings place on them. Furthermore, we have synthesised this evidence to develop a value proposition to facilitate decision-making around their integration into sexual healthcare. By reviewing the Cepheid CT/NG GeneXpert’s implementation, we were able to demonstrate the diversity of use in various healthcare settings (specialist, non-specialist, and outreach), and in different areas of the world, allowing a more robust review of the test’s value from multiple stakeholder perspectives.
Of particular interest is the finding that sexual health specialist and outreach services had the least overlap in values. This underlines the need for specific measures of value to be identified by service type: if a service does not already exist (as in outreach), mapping outcome measures such as costs of changes to existing clinical pathways and associated costs of task redeployment are redundant, whereas these are clearly important measures if redesigning an existing sexual health clinic service. Similarly, consideration of existing services provided within specific settings matter: measuring the impact of replacing traditional laboratory CT/NG NAATs with POCTs (including impact on current laboratory contracts) requires different evaluation indicators than does the replacement of syndromic management of possible infections with POCTs. The examples presented here highlight our key finding: the value of novel diagnostic test adoption and implementation is perceived differently depending on your setting and stakeholder role. It is therefore critical for the values for the specific service to be identified before a test and its mode of implementation are chosen.
We did not consider studies that focused solely on test performance, or reports on test implementation in research-use-only environments, as we considered these outside the remit of this report. By limiting ourselves to implementation studies, we may have missed identifying additional values of the test, although we tried to address this by including research study outcomes in the final value proposition (Table 4). We only searched two databases (Medline and Embase), but given the subject area, the inclusion of conference abstracts, and the fact we searched references of included papers, we think all relevant publications have been identified. It is likely, however, that there are other cases of implementation that have not been reported in the literature; publications available will most likely reflect the values of the study authors, and not those of all stakeholders involved. Furthermore, multiple value propositions for POCTs exist [34, 35]; we chose one, based on its relevance to laboratory medicine and inclusion of diversity of stakeholder values.
We found variability between reports of implementation studies and their outcomes, as well as in their study quality. Not all of the studies included reported on clinical pathways (i.e. procedures), which would have outlined how the test was used. As a result, we cannot directly compare the results of each setting, which precluded metanalysis and limits our ability to understand the value of the test to each stakeholder in each of the different contexts. We encourage authors to have clear objectives, to report on outcomes matching these objectives, and to follow the appropriate international standards of reporting for their chosen study design. However, although uniformity would enable better evaluation across different settings, it would unlikely reflect the diversity of outcomes that need to be measured in those different settings; the heterogeneity in study design, test implementation and impacts assessed in the literature in itself demonstrates the variability of values placed on molecular CT/NG POCTs by different stakeholders and in different settings. For example, the inclusion of qualitative studies in the value proposition we propose enabled us to broaden our understanding of the contextual values of these POCTs. We suggest more work be done to understand the values of a wider variety of stakeholders in order to encourage them to be actively involved in study design and implementation, which would lead to reporting of more relevant outcomes of interest. We also encourage reflexive reporting on lessons learned, particularly with regards to study design and outcomes measures; if any data were found to be important when assessing the POCTs for adoption but were not thought to be important when the evaluation was designed, this would be useful to consider in future studies and their design.
Despite the diversity of Cepheid CT/NG GeneXpert implementation mechanisms, there were commonalities among study outcomes to explore. Patient benefit was measured in each, although the indicators that were measured varied, including numbers of patients who received a same-day result, time between clinic visit and/or sample taking and result provision, and patient acceptability. Among CT/NG positive patients, time to treatment, and partner notification/treatment measures were also commonly reported.
Healthcare professionals are a particularly important stakeholder group for implementation and previous research to identify an ideal test has focused on them [80]; clinicians are often responsible for new pathway construction [52, 81], and research has shown that nurses’ inclusion in quality improvement projects may improve job satisfaction and reduce workforce instability [82]. Healthcare providers across the included studies placed value in patient benefits, specifically the reduced time to result notification, and for those patients testing positive, reduced time to treatment. Qualitative studies, in particular those among healthcare professionals participating in the TTANGO studies in Australia, reported high levels of satisfaction with the Cepheid CT/NG GeneXpert, and related this to their belief in the test’s ability to improve patient and public health outcomes, as well as the device’s ease of use [83, 84]. However, in some studies [61, 65], the faster time to results delivery was negatively impacted by patients being unwilling or unable to wait for their results at the point of care; qualitative studies providing insight into the appropriate implementation of CT/NG POCTs into routine healthcare practice may help to mitigate this issue [85].
No test fulfils all the WHO TPP or (RE)ASSURED criteria [9, 11, 12]. However, even less-than-perfect technologies have the potential to improve patient outcomes [86, 87]; waiting for the ideal molecular POCT before implementing tests that are currently available has implications both for individual patients and public health [88, 89]. This research synthesis shows the potential for less-than-perfect CT/NG POCTs to hold value for multiple stakeholders in different healthcare settings. Therefore, we recommend that stakeholders in sexual healthcare explore the potential for existing POCTs to provide value to their services. As more molecular CT/NG POCTs are developed and approved by regulatory bodies, the specific characteristics of each may be more or less suited to particular settings, and the value proposition developed could help decision-makers determine the most important values for them and their stakeholders to guide test choice.
Conclusions
Criteria have been set for the development of ideal CT/NG POCTs. Similarly, guidance has been developed for the adoption of novel diagnostics into health systems. This guidance is necessary to protect patients and direct health systems towards efficient use of resources to meet public health goals, and attempts to cater to a diverse range of stakeholder needs and expectations. The plurality of these needs means that a single test is unlikely to be viewed as a panacea or “magic bullet” for solving the clinical, social and structural issues around provision of CT/NG diagnosis across all settings. Stakeholders wishing to improve their service through the implementation of CT/NG POCTs should be supported to identify the values most relevant to their settings and context rather than waiting for the ideal test to be produced: there is no magic bullet.
Supporting information
S3 Table. Quality assessment for all included articles, by article, article type, score and percentage and location in manuscript tables.
https://doi.org/10.1371/journal.pone.0259593.s003
(DOCX)
S4 Table. Service evaluation article assessment.
https://doi.org/10.1371/journal.pone.0259593.s004
(DOCX)
S5 Table. Before and after study article assessment.
https://doi.org/10.1371/journal.pone.0259593.s005
(DOCX)
S6 Table. Randomised controlled trial study article assessment.
https://doi.org/10.1371/journal.pone.0259593.s006
(DOCX)
S7 Table. Qualitative study article assessment.
https://doi.org/10.1371/journal.pone.0259593.s007
(DOCX)
S8 Table. Questionnaire study article assessment.
https://doi.org/10.1371/journal.pone.0259593.s008
(DOCX)
Acknowledgments
Special thanks to Professors Christopher Price and Trisha Greenhalgh for organising the Maximising Value from New Diagnostic Tests workshop in 2019, which inspired this publication.
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