https://orcid.org/0000-0003-0076-0985
Figures
Abstract
Introduction
Although Clinical Practice Guidelines (CPG) highlight that laparoscopy is often used in the treatment of endometriosis, its diagnostic usefulness is not fully defined. Our objective was to evaluate the quality of CPGs for endometriosis that address the use of diagnostic laparoscopy in reproductive age women, and describe the recommendations and methods used to assess diagnostic test questions.
Methods
A comprehensive search of 5 databases (Trip Database, MEDLINE/PubMed, Web of Science, SCOPUS, and EMABSE) and websites of guideline development organizations and compilers was conducted from 2017 to 2023. A descriptive analysis of the recommendations was performed and the quality of the guidelines was assessed using the AGREE-II instrument.
Results
Four CPGs were included in the review, all exhibiting adequate methodological quality (scores ranging from 66.7% to 91.0%). Regarding the use of laparoscopy for endometriosis diagnosis, discrepancies in recommendations were observed. Two guidelines advised against it, one recommended either laparoscopy or medical empirical treatment, and one favored its use. GRADE guidance was employed for evidence assessment, but only one guideline transparently reported the certainty of evidence and the evidence-to-decision framework process.
Conclusions
Variability in recommendations among different CPGs were found. To keep in mind, discrepancies arise from differing prioritizations of the assessment of clinical impact in patient important outcomes and methodological approaches. This underscores the need for more standardized and transparent guideline development processes, particularly in addressing the clinical utility of diagnostic tests.
Citation: Zela-Coila F, Quispe-Vicuña C, Nuñez-Lupaca JN, Aparicio-Curazi M, Goicochea-Lugo S (2024) Comparison of clinical practice guidelines methods to reach diagnostic test recommendations regarding diagnostic laparoscopy for endometriosis: A scoping review. PLoS ONE 19(12): e0310593. https://doi.org/10.1371/journal.pone.0310593
Editor: Diego Raimondo, Dipartimento di Scienze Mediche e Chirugiche (DIMEC), Orsola Hospital, ITALY
Received: April 25, 2024; Accepted: August 22, 2024; Published: December 11, 2024
Copyright: © 2024 Zela-Coila 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 author(s) received no specific funding for this work.
Competing interests: The authors have declared that no competing interests exist.
Introduction
Endometriosis affects 10% of reproductive-age women worldwide and is characterized by chronic pain and infertility [1–3]. However, diagnosing endometriosis remains challenging, involving a delay of 6 to 11.7 years [4–7]. While laparoscopy is considered the reference standard based on its results in diagnostic accuracy outcomes, it is important to consider the certainty of these results, the operator-dependent accuracy [8] and to keep in mind that the effects on clinically important outcomes for patients should also be known [9]. Additionally, laparoscopy is an invasive, expensive procedure, difficult to access in certain contexts, which is not devoid of complications, and there may be other alternatives to the use of laparoscopy as a diagnostic test that are non-invasive, such as empirical medical treatment [10, 11].
Clinical practice guidelines (CPGs) can address these types of uncertain scenarios by issuing recommendations based on systematic searches and appropriate methodological procedures to resolve questions about the use of diagnostic tests. In this regard, the Grading of Recommendations, Assessment, Development and Evaluation (GRADE) methodology proposes methodological guidelines for addressing this type of clinical questions, emphasizing decision-making on the clinical impact of diagnostic test such as laparoscopy on clinically important outcomes for patients, and considering a transparent multicriteria framework for issuing recommendations [12–16].
Prioritizing or not the decision-making process based on the clinical impact of the use of diagnostic tests, as well as employing different methods for issuing recommendations and properly adhering to them, can lead to contradictory recommendations among CPGs. In consequence, this study aims to evaluate the quality of CPGs for endometriosis that address the use of diagnostic laparoscopy, analyzing recommendations and methods to reach recommendations for this type of clinical question.
Methods
We performed a scoping review following the methodology detailed by the Joanna Briggs Institute [17], following the guidelines of the Preferred Reporting Items for Systematic and Meta-Analysis extension for Scoping Reviews (PRISMA-ScR) [18] (S1 Table), and registered the study protocol in the repository Figshare [19].
Eligibility criteria
We included only evidence-based clinical practice guidelines (CPG), defined as a document that formulates recommendations based on systematic reviews of the literature, that provide recommendations regarding the use of laparoscopy for the diagnosis of pelvic endometriosis in reproductive age women with endometriosis, published or fully/partially updated during 2017 to 2023, and were available in English or Spanish language.
We excluded guidelines whose recommendations are adopted or adopted, and those whose methodology and recommendations cannot be obtained in full text. In addition, we excluded systematic reviews, observational studies, clinical trials, conference abstracts, letters to the editor, and case reports.
Information sources and search strategy
We searched in databases (Trip Database, MEDLINE/PubMed, Web of Science, SCOPUS, and EMBASE), web pages of guideline development organizations (Scottish Intercollegiate Guidelines Network [SIGN], National Institute for Health and Care Excellence [NICE], Australian Clinical Practice Guidelines, New Zealand Guidelines Group, Centro Nacional de Excelencia Tecnológica en Salud [CENETEC], Guías Salud, Instituto de Evaluación de Tecnologías en Salud e Investigación [IETSI], and the American College of Physicians Clinical Practice Guidelines), and web pages of guideline compilers (Canadian Medical Association Infobase, Base Internacional de Guías GRADE, Guidelines International Network, National Guideline Clearinghouse, EGuideline, and Best Practice Guideline); from January 1st, 2017, to July 23th, 2023. Complete search strategy for each database in S2 Table.
Study selection
We imported the articles from databases into Rayyan software, where duplicates were manually removed. Then, the obtained results were merge with articles sourced from guideline development organization web pages and guideline compilers, followed by a second manual removal of duplicates. Subsequently, four researchers (JNL, FZC, MAC, CQV) independently screened titles and abstracts to identify potentially relevant articles for inclusion. These potential articles were found and full text reviewed independently by the same researchers to verify compliance with the inclusion criteria. The disagreements were resolved with a fifth researcher (SGL).
Data extraction
Four researchers (JNL,FZC,MAC,CQV) independently extract the following information from each included guideline: CPGs characteristics (organization, year, country, perspective, scope, method used to assess the certainty of the evidence and its definition, system to classify the strength of recommendations and its definition, and funding), characteristics regarding the recommendations on the use of laparoscopy for the diagnosis of endometriosis, and the methods used to assess diagnostic test clinical questions. In addition, we performed the quality appraisal of each CPG.
Quality appraisal
We used the Appraisal of Guidelines Research and Evaluation II (AGREE-II) instrument [20], which includes 23 items distributed in six domains (scope and purpose, involvement of stakeholders, rigor of development, clarity, and presentation, applicability, and editorial independence) to assess the quality of CPGs. Three researchers (forming groups distributed between JNL, FZC, MAC, CQV) independently rated each item on a seven-point scale from strongly disagree (score 1) to strongly agree (score 7). When a difference of two or more points was found in one of the items between researchers, a fifth researcher (SGL) solved the disagreement and reach a consensus. Then we followed the AGREE-II guidelines to calculate the global score for each domain ranging from 0 to 100%, where higher score indicates better quality.
The guideline of the instrument does not provide a minimum domain score to classify the quality of the guidelines. In consequence, we used a cut-off point based on previous studies that evaluated the quality of GPCs in gynecology and obstetrics topics [21, 22]. We considered that a CPG had an adequate quality when all six domains had a score ≥ 60%, and an adequate methodological quality when the third domain (rigor of development) had a score ≥ 60%.
Appraisal of recommendations and methods to assess diagnostic test questions in CPGs
We extracted recommendations regarding the use of laparoscopy for the diagnosis of endometriosis from each CPG and described the following characteristics: recommendation (as state in the CPG), direction, strength, and certainty of the evidence. In addition, we described the methods used to reach the recommendations.
To our best knowledge, there is no specific validated tool for reporting and appraising methods to assess diagnostic test questions in CPGs. We utilized the GRADE guidelines as a reference standard methodology for formulating recommendations on this type of questions. GRADE was chosen due to its explicit steps guiding guideline developers in assessing the certainty of evidence for test accuracy, transitioning from test accuracy to patient-important outcomes, and making recommendations about diagnostic tests using multicriteria frameworks [12–16].
In based on that, we analyzed and described the following methodological characteristics: procedures to generate clinical question and decide on the importance of outcomes (clinical question, PICO framework, role of the diagnostic test, assessment of patient important outcomes or consequences of correct/incorrect classification), perform the systematic review of the evidence and determine the certainty of the evidence (databases and date of search, restrictions, type of study to be search, tool to assess risk of bias or quality of studies, method or criteria to determine certainty of evidence), prepare and report summaries of evidence tables (type of evidence table used, pre-test probability, principal results), and to discuss evidence to decision criteria (EtD table use, benefits, harms, certainty of the evidence, values and preferences, balance between benefits and harms, resource use or cost-effectiveness, equity, acceptability, feasibility).
Results
Study selection
We identified 4353 records from systematic search. After removed duplicates, 2479 records were screened by title and abstract, resulting in 54 records to evaluate full text for eligibility. We excluded 50 records after full text analysis and finally 4 CPGs were included. In addition, no other guideline was added from the citation searching of the included CPGs. Fig 1 presents the flow diagram of CPG selection in detail and the list of excluded articles and reasons for exclusion is available in S3 Table.
The included CPG were: “Guía de práctica clínica para el diagnóstico y tratamiento de la endometriosis sintomática en mujeres en edad reproductiva” developed by IETSI (IETSI-2022) [23], “Endometriosis” developed by European Society of Human Reproduction and Embryology (ESHRE-2022) [11], “Manejo de la paciente con endometriosis en la edad fértil” developed by Sociedad Española de Fertilidad (SEF-2018) [24], and Endometriosis: diagnosis and management” developed by NICE (NICE-2017) [25].
Study characteristics
The CPG were developed in Peru [23], Spain [24], United Kingdom [25], and in a collaboration between European countries [11]. The perspective was not reported in three of four (3/4) guidelines [11, 24, 25], and one guideline used a population perspective [23]. The main scope for guideless was diagnosis and treatment. Two of four (2/4) guidelines were published in 2022 [11, 23]. All CPG used GRADE as the method to assess the certainty of the evidence and three of four (3/4) CPG used GRADE as the system to classify the strength of recommendations. Definitions for the certainty of the evidence, strength of recommendations and the terminology used to phrase the strength of the recommendations varied among the guidelines. In addition, two guidelines were funded by public funds [23, 25], and the remaining ones did not report the source of funding [11, 24]. Table 1 presents the characteristics and definitions used by CPG in detail.
Quality appraisal of CPGs
Only one guideline (NICE-2017) [25] had an adequate quality in all domains of AGREE-II and all the CPG had an adequate methodological quality. In this sense, the CPG with the highest score was IETSI-2022 (91.0%) [23], while the one with the lowest score was SEF-2018 (66.7%) [24]. Table 2. Presents the quality appraisal of guidelines in detail.
Synthesis of results
Recommendations regarding the use of diagnostic laparoscopy.
Two guidelines state recommendations against the use of laparoscopy to diagnose endometriosis (IETSI-2022 and SEF-2018) [23, 24], one guideline state a recommendation for either the use of diagnostic laparoscopy or medical empirical treatment (ESHRE-2022) [11], and one guideline state a recommendation in favor the use of laparoscopy to diagnose endometriosis (NICE-2017) [25]. The strength of recommendations was conditional in three guidelines (IETSI-2022, SEF-2018, and NICE-2017) [23–25] and not reported in one guideline (ESHRE-2022) [11]. Finally, the certainty of the evidence for the recommendations was not reported in two guidelines, state as very low in one guideline (IETSI-2022) [23], and state as high in one guideline (SEF-2018) [24]. Table 3 details characteristics and methodological steps for each guideline.
Generation of the clinical question generation and determination of the importance of outcomes
Two guides did not fully report information for all components of the PICO framework (SEF-2018 and NICE-2017) [24, 25]. The population of interest were reproductive-age women with suspected endometriosis for all guidelines. However, only one guideline specified details regarding the use of previous diagnostic tests and the type of endometriosis (IETSI-2022) [23]. Diagnostic laparoscopy was the intervention of interest in all guidelines but only one guideline specified the role of the test (IETSI-2022) [23]. Empirical medical treatment was the comparator in two guidelines (IETSI-2022 and ESHRE-2022) [11, 23]. Clinical benefits and complications or consequences of correct/incorrect classification were outcomes of interest in two guidelines (IETSI-2022 and ESHRE-2022) [11, 23], diagnostic test accuracy were outcomes of interest in two guidelines (IETSI-2022 and NICE-2017) [23, 25], and one guideline did not specify prioritized outcomes.
Regarding importance of outcomes, two guidelines did not report the importance of outcomes. The clinical patient important outcomes were at least important in one guideline (IETSI-2022) [23] and diagnostic test accuracy outcomes were critical in the remaining one (NICE-2017) [25].
Systematic review of the evidence and certainty of the evidence assessment
All guidelines searched at least two databases and the date of search varied between 2016 to 2022. Three guidelines applied language restrictions, while this information was not reported by one guideline (SEF-2018) [24]. All CPG searched systematic reviews; three guidelines proposed searching for RCT; and one guideline prioritized searching for diagnostic accuracy observational studies (NICE-2017) [25]. All guidelines planned to use an instrument for risk of bias or study quality assessment, but only two guidelines specified QUADAS-2 (IETSI-2022 and NICE-2017) [23, 25]. Regarding the certainty of evidence assessment, all guidelines mentioned using the GRADE methodology.
Preparation and report summaries of evidence tables with principal results
Only one guideline used SoF tables to report summaries of evidence and report the pre-test probability for the target condition (IETSI-2022) [23]. In general, guidelines mentioned a lack of studies on the clinical impact of using diagnostic laparoscopy. Sensitivity and specificity values were reported by three guidelines and showed slight variations (IETSI-2022, SEF-2018, and NICE-2017) [23–25] ranging from 0.94 to 0.98 for sensitivity and 0.79 for specificity. However, only one guideline explicitly addressed the clinical consequences of correct/incorrect classification with diagnostic laparoscopy and express it in number of cases per 100 individuals (IETSI-2022) [23]. In addition, two guidelines report the incidence of complications of the procedure, ranging from 2.3% to 6.8% (IETSI-2022 and ESHRE-2022) [11, 23].
The certainty of the evidence was appropriately expressed using the GRADE terminology in only one guideline and stated as low to very low certainty of the evidence (IETSI-2022) [23]. The remaining guidelines highlighted study limitations based on the risk of bias, using terms like "methodological limitations" or "high risk of bias", or based on the indirectness of the evidence, but did not detail the assessment of the remaining criteria proposed by GRADE.
Discussion regarding evidence to decision criteria and reporting using a EtD table
Only one guideline used the EtD table to report the discussion regarding evidence to decision criteria and explicitly report the judgement for each criterion as proposed by GRADE (IETSI-2022) [23].
Regarding benefits, two guidelines, IETSI-2022 and ESHRE-2022, focused on potential clinical effects [11,23], one on laparoscopy’s diagnostic accuracy (NICE-2017) [25], and the last, SEF-2018 [24], did not discuss benefits. IETSI-2022 considered benefits trivial, emphasizing empirical therapy’s comparable advantages for high pre-test probability cases. ESHRE-2022 highlighted a lack of evidence for laparoscopy’s superiority over empirical treatment.
Regarding harms, two guidelines discussed the consequences of incorrect classification or potential complications of laparoscopy concerning harms (IETSI-2022 and ESHRE-2022) [11,23], while others did not address this criterion. IETSI-2022 found harms to be trivial due to infrequent and not severe consequences, and ESHRE-2022 [11] highlighted the need to consider potential risks without explicitly judging this criterion.
Regarding the overall certainty of the evidence and the balance between benefits and harms, only one guideline reported the judgment for this criterion using the terminology proposed by GRADE (IETSI-2022) [23]. For IETSI-2022 [23] guideline, the overall certainty of the evidence was very low, and the balance possibly does not favor either the use of diagnostic laparoscopy or the empirical medical treatment in based of previous judgements for benefits, harms, and the certainty of the evidence. Similarly, ESHRE-2022 [11] guideline mention that there is no evidence of superiority of either approach and psychological benefits of a confirmed diagnosis should be weight against the value and risk of diagnostic laparoscopy. In contrast, SEF-2018 [24] guideline mention that the evidence on diagnostic accuracy of laparoscopy for endometriosis had limitations and there are empirically effective and safe treatments for symptom management. Finally, NICE-2017 [25] did not report discussions for this criterion.
Regarding resource use or cost-effectiveness, only one guideline reports the judgement for this criterion using the terminology proposed by GRADE (IETSI-2022) [23]. The IETSI-2022 [23] guideline, assess the costs associated with the use of diagnostic laparoscopy and concluded moderate costs. The ESHRE-2022 [11] guidelines classified the diagnostic laparoscopy as “expensive” and NICE-2017 [25] guidelines conducted an economic model, considering the limitations of assuming that diagnostic laparoscopy is the “gold standard”, and concluded that is a cost-effective form of diagnosis. Nevertheless, mention that when taken as one of many possible diagnosis/treatment strategies, surgical diagnosis is not preferred to empirical diagnosis and not expensive treatment. In addition, SEF-2018 [24] guideline did not report discussion for this criterion.
Regarding the remaining criteria, patient values and preferences were discussed by three guidelines (IETSI-2022, ESHRE-2022, and NICE-2017) [11,23,25], the impact on health equity was discussed by one guideline (probably reduced) (IETSI-2022) [23], the acceptability of laparoscopy was discussed by two guidelines (varies) (IETSI-2022 and ESHRE-2022) [23,25], and feasibility was discussed by one guideline (likely feasible in specialized centers but may not be available in other regions in the short term) (IETSI-2022) [23].
Discussion
In our analysis, despite a similar body of evidence on laparoscopy’s diagnostic accuracy, guidelines exhibited divergent recommendations. Variability in prioritizing outcomes, especially clinical benefits or consequences on patient-important outcomes, may contribute to these differences. While there’s a proposed need for Clinical Practice Guidelines (CPGs) to evaluate the clinical impact of a test, our review indicates that this approach is not commonly practiced. A study analyzing 15 guidelines found that out of 15 recommendations on diagnostic test use, only 3 considered the effectiveness of treatments following the tests, and none linked the diagnostic test results with the decision-making process for subsequent treatment administration [9].
Guideline recommendations vary due to inconsistent consideration of criteria in transitioning from evidence to decision and variability in how guidelines address and weigh these criteria. The balance between benefits and harms, along with evidence certainty, is crucial in shaping the initial recommendation direction and is often considered in guidelines [26]. In our results, only one guideline comprehensively assessed the potential benefits by evaluating the absolute effects of accurate laparoscopy classification in women with a clearly defined high pre-test probability. This guideline also effectively communicated the certainty of the evidence for these outcomes, an important aspect considering that the magnitude of benefits can varied according to the initial probability of the condition [15]. Furthermore, only two guidelines addressed potential harms. This lack of emphasis on the burden of diagnostic tests and the methodological shortcomings in gathering such information have been previously noted. A study highlighted that only 3 of 15 guidelines reviewed considered the harm burden related to diagnostic tests, and this consideration was not supported by systematic searches for evidence [9].
The balance of effects and certainty of evidence results must be weighed against other EtD framework criteria for the final recommendation. Considerations on resource use or cost-effectiveness, crucial in decision-making, vary based on contextual factors [27]. In this regard, our analysis found that guidelines assigned different importance to resource use in issuing their recommendations. The variability in the importance given by the guidelines to the discussion of this criterion could be explained by the perspective of the guidelines. For instance, for guidelines with a population perspective, resource use must justify the magnitude of the benefits found to issue a favorable recommendation; otherwise, it is more likely to issue a recommendation against it, as reported by the IETSI-2022 guideline. The limited information on the perspective of the included guidelines does not allow for a more detailed understanding of the importance assigned to each criterion. This lack of information aligns with findings from a study in which only 24% of guidelines from various health areas reported the perspective to be used [26].
All guidelines used GRADE to assess evidence certainty and issue recommendations. However, only one complied with reporting and explaining certainty in detail, using GRADE’s recommended phrasing and terminology. Utilizing SoF tables aids quick and improved interpretation for decision-making [28]. Furthermore, the EtD table is one of the most frequently used decision frameworks [26], and its use allows guiding decision-making through multiple criteria in a systematic, explicit, and transparent way to issue recommendations, stating their direction and strength [29]. In the evaluation of EtD criteria within clinical guidelines, equity, acceptability, and feasibility were the least addressed, aligning with a study that found these criteria discussed in only 16%, 28%, and 34% of 68 guidelines, respectively [26].
Despite adequate overall methodological quality, not all guidelines consistently applied GRADE methodology. The most GRADE-adherent guideline scored highest in the third domain. This aligns with a study on 15 Australian guidelines, indicating inconsistent GRADE application (73.3%). However, those closely following GRADE achieved higher methodological rigor scores. The authors noted that 40% of the guidelines failed to report sufficient information on the importance of outcomes, 13% did not use GRADE’s evidence certainty categories, 47% did not present results using evidence summary tables, and 80% did not present the EtD framework. Challenges in applying GRADE to assess clinical impact of diagnostic tests include skepticism on recommendation strength, a preconceived confidence in benefits despite low evidence certainty, and limitations in guideline development groups’ understanding of the methodology [30]. However, published case analyses on diagnostic test questions can guide these groups [31]. Additionally, the GRADE series offers several articles clarifying the steps to make recommendations on diagnostic tests and there exists publications about how to use the EtD frameworks [32]. More articles are being published to operationalize the evaluation of criteria for making a recommendation, which improve the interrater agreement for making a for/against recommendation [33]. The analysis table we present in this article is also available for use as a tool to verify the report and analyze the consistency of the recommendation on the use of a diagnostic test. Finally, educational programs are available on the GRADE Working Group website (https://www.gradeworkinggroup.org/) to enhance the training of guideline development groups in using these methods and improving their understanding.
Despite the above, although laparoscopy reports good diagnostic and therapeutic utility in the clinical recommendations, some endometriotic lesions may be missed because some implants may be very small or hidden to white light laparoscopy, so near infrared radiation (NIR) intraoperative imaging technology has shown to be a useful tool in these situations [34]. In addition to this, it has been reported that a miRNA pattern could be a promising and cost-effective tool for the diagnosis of endometriotic implants in patients with or without symptoms, mainly by liquid biopsy [35]. Therefore, these considerations should be taken into account in the development of future clinical recommendations for patients with endometriosis.
Strengths and limitations
This study analyzed four CPGs based on methodology indicators like recommendation characteristics, diagnostic test question approach, PICO structure, evidence search, limitations assessment, evidence synthesis, and transition to recommendation. The AGREE instrument guided the appraisal. Limitations include the inability to access dynamic panel information, explaining decisions and transparency gaps due to document analysis.
Conclusions
This scoping review highlights the variability in recommendations for diagnostic laparoscopy in endometriosis among different CPGs. Despite similar evidence on diagnostic accuracy, discrepancies stem from differing prioritizations of clinical impact assessment and methodological approaches. There’s a need for standardized and transparent guideline development processes, especially addressing the clinical utility of diagnostic tests.
Supporting information
S1 Table. PRISMA extension for Scoping Reviews (PRISMA-ScR) checklist.
https://doi.org/10.1371/journal.pone.0310593.s001
(DOCX)
References
- 1. Parasar P, Ozcan P, Terry KL. Endometriosis: Epidemiology, Diagnosis and Clinical Management. Curr Obstet Gynecol Rep. 2017;6(1):34–41. pmid:29276652
- 2. Shafrir AL, Farland LV, Shah DK, Harris HR, Kvaskoff M, Zondervan K, et al. Risk for and consequences of endometriosis: A critical epidemiologic review. Best Practice & Research Clinical Obstetrics & Gynaecology. 2018;51:1–15.
- 3. Carbone MG, Campo G, Papaleo E, Marazziti D, Maremmani I. The Importance of a Multi-Disciplinary Approach to the Endometriotic Patients: The Relationship between Endometriosis and Psychic Vulnerability. J Clin Med. 2021;10(8):1616. pmid:33920306
- 4. Nnoaham KE, Hummelshoj L, Webster P, d’Hooghe T, de Cicco Nardone F, de Cicco Nardone C, et al. Impact of endometriosis on quality of life and work productivity: a multicenter study across ten countries. Fertil Steril. 2011;96(2):366–373.e8. pmid:21718982
- 5. Hudelist G, Fritzer N, Thomas A, Niehues C, Oppelt P, Haas D, et al. Diagnostic delay for endometriosis in Austria and Germany: causes and possible consequences. Hum Reprod. 2012;27(12):3412–6. pmid:22990516
- 6. Arruda MS, Petta CA, Abrão MS, Benetti-Pinto CL. Time elapsed from onset of symptoms to diagnosis of endometriosis in a cohort study of Brazilian women. Hum Reprod. 2003;18(4):756–9. pmid:12660267
- 7. Hadfield R, Mardon H, Barlow D, Kennedy S. Delay in the diagnosis of endometriosis: a survey of women from the USA and the UK. Hum Reprod. 1996;11(4):878–80. pmid:8671344
- 8. Simko S, Wright KN. The future of diagnostic laparoscopy–Cons. Reprod Fertil. 2022;3(2):R91–5. pmid:35706581
- 9. Tuut MK, Burgers JS, van der Weijden T, Langendam MW. Do clinical practice guidelines consider evidence about diagnostic test consequences on patient‐relevant outcomes? A critical document analysis. J Eval Clin Pract. 2022;28(2):278–87. pmid:34553815
- 10. Albee RB, Sinervo K, Fisher DT. Laparoscopic excision of lesions suggestive of endometriosis or otherwise atypical in appearance: relationship between visual findings and final histologic diagnosis. J Minim Invasive Gynecol. 2008;15(1):32–7. pmid:18262141
- 11.
European Society of Human Reproduction and Embryology. ESHRE Guideline Endometriosis [Internet]. 2022 [citado 4 de mayo de 2023]. Disponible en: https://www.eshre.eu/Guideline/Endometriosis
- 12. Schünemann HJ, Mustafa R, Brozek J, Santesso N, Alonso-Coello P, Guyatt G, et al. GRADE Guidelines: 16. GRADE evidence to decision frameworks for tests in clinical practice and public health. J Clin Epidemiol. 2016;76:89–98. pmid:26931285
- 13. Schünemann HJ, Mustafa RA, Brozek J, Steingart KR, Leeflang M, Murad MH, et al. GRADE guidelines: 21 part 1. Study design, risk of bias, and indirectness in rating the certainty across a body of evidence for test accuracy. J Clin Epidemiol. 2020;122:129–41. pmid:32060007
- 14. Schünemann HJ, Mustafa RA, Brozek J, Steingart KR, Leeflang M, Murad MH, et al. GRADE guidelines: 21 part 2. Test accuracy: inconsistency, imprecision, publication bias, and other domains for rating the certainty of evidence and presenting it in evidence profiles and summary of findings tables. J Clin Epidemiol. 2020;122:142–52. pmid:32058069
- 15. Schünemann HJ, Mustafa RA, Brozek J, Santesso N, Bossuyt PM, Steingart KR, et al. GRADE guidelines: 22. The GRADE approach for tests and strategies-from test accuracy to patient-important outcomes and recommendations. J Clin Epidemiol. 2019;111:69–82. pmid:30738926
- 16. Yang B, Mustafa RA, Bossuyt PM, Brozek J, Hultcrantz M, Leeflang MMG, et al. GRADE Guidance: 31. Assessing the certainty across a body of evidence for comparative test accuracy. J Clin Epidemiol. 2021;136:146–56. pmid:33864930
- 17. Peters MDJ, Godfrey CM, Khalil H, McInerney P, Parker D, Soares CB. Guidance for conducting systematic scoping reviews. International Journal of Evidence-Based Healthcare. 2015;13(3):141–6. pmid:26134548
- 18. Tricco AC, Lillie E, Zarin W, O’Brien KK, Colquhoun H, Levac D, et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation. Ann Intern Med. 2018 Oct 2;169(7):467–473. pmid:30178033
- 19. Nuñez-Lupaca JN, Aparicio-Curazi MM, Zela-Coila F, Quispe-Vicuña C, Goicochea-Lugo S. Diagnostic laparoscopy for endometriosis: A review of clinical practice guideline recommendations—Protocol. 2022;556823 Bytes.
- 20. AGREE Enterprise Website. AGREE-REX: Recommendation EXcellence—AGREE Enterprise website [Internet]. [citado 4 de mayo de 2023]. Disponible en: https://www.agreetrust.org/resource-centre/agree-rex-recommendation-excellence/
- 21. Nygaard CC, Tsiapakidou S, Pape J, Falconi G, Betschart C, Pergialiotis V, et al. Appraisal of clinical practice guidelines on the management of obstetric perineal lacerations and care using the AGREE II instrument. Eur J Obstet Gynecol Reprod Biol. 2020;247:66–72. pmid:32070848
- 22. Ghai V, Subramanian V, Jan H, Loganathan J, Doumouchtsis SK. Evaluation of clinical practice guidelines (CPG) on the management of female chronic pelvic pain (CPP) using the AGREE II instrument. Int Urogynecol J. 2021;32(11):2899–912. pmid:34148114
- 23. Instituto de Evaluación de Tecnologías en Salud e Investigación (IETSI). Guía de práctica clínica para el diagnóstico y tratamiento de la Endometriosis sintómatica en mujeres en edad reproductiva—GPC [Internet]. 2022 [citado 3 de septiembre de 2023]. Disponible en: https://gpc-peru.com/endometriosis
- 24. Carrera M, Domínguez J, Pérez Milán F, Gris J, Caballero M, Álvarez C, et al. Manejo de la paciente con endometriosis durante la edad fértil. Guía de práctica clínica basada en la evidencia 2018 SEF. 2018; Disponible en: https://www.sefertilidad.net/newsletter/newsletter135.html
- 25.
NICE guideline. Overview | Endometriosis: diagnosis and management | Guidance | NICE [Internet]. NICE; 2017 [citado 4 de mayo de 2023]. Disponible en: https://www.nice.org.uk/guidance/ng73
- 26. Meneses-Echavez JF, Bidonde J, Yepes-Nuñez JJ, Poklepović Peričić T, Puljak L, Bala MM, et al. Evidence to decision frameworks enabled structured and explicit development of healthcare recommendations. J Clin Epidemiol. 2022;150:51–62. pmid:35710054
- 27. Brunetti M, Shemilt I, Pregno S, Vale L, Oxman AD, Lord J, et al. GRADE guidelines: 10. Considering resource use and rating the quality of economic evidence. J Clin Epidemiol. 2013;66(2):140–50. pmid:22863410
- 28. Rosenbaum SE, Glenton C, Oxman AD. Summary-of-findings tables in Cochrane reviews improved understanding and rapid retrieval of key information. J Clin Epidemiol. 2010;63(6):620–6. pmid:20434024
- 29. Li SA, Alexander PE, Reljic T, Cuker A, Nieuwlaat R, Wiercioch W, et al. Evidence to Decision framework provides a structured «roadmap» for making GRADE guidelines recommendations. J Clin Epidemiol. 2018;104:103–12. pmid:30253221
- 30. Alexander PE, Gionfriddo MR, Li SA, Bero L, Stoltzfus RJ, Neumann I, et al. A number of factors explain why WHO guideline developers make strong recommendations inconsistent with GRADE guidance. J Clin Epidemiol. 2016;70:111–22. pmid:26399903
- 31. Hsu J, Brożek JL, Terracciano L, Kreis J, Compalati E, Stein AT, et al. Application of GRADE: Making evidence-based recommendations about diagnostic tests in clinical practice guidelines. Implementation Science. 2011;6(1):62. pmid:21663655
- 32. Moberg J, Oxman AD, Rosenbaum S, Schünemann HJ, Guyatt G, Flottorp S, et al. The GRADE Evidence to Decision (EtD) framework for health system and public health decisions. Health Res Policy Syst. 2018;16(1):45. pmid:29843743
- 33. Kumar A, Miladinovic B, Guyatt GH, Schünemann HJ, Djulbegovic B. GRADE guidelines system is reproducible when instructions are clearly operationalized even among the guidelines panel members with limited experience with GRADE. J Clin Epidemiol. 2016;75:115–8. pmid:26845745
- 34. Vizzielli G, Cosentino F, Raimondo D, Turco LC, Vargiu V, Iodice R, et al. Real three-dimensional approach vs two-dimensional camera with and without real-time near-infrared imaging with indocyanine green for detection of endometriosis: A case-control study. Acta Obstet Gynecol Scand. 2020;99(10):1330–8. pmid:32274789
- 35. Ronsini C, Fumiento P, Iavarone I, Greco PF, Cobellis L, De Franciscis P. Liquid Biopsy in Endometriosis: A Systematic Review. Int J Mol Sci. 2023;24(7):6116. pmid:37047088