Endometriosis classification systems: an international survey to map current knowledge and uptake

In the field of endometriosis, several classifications, staging and descriptive systems have been developed, however, none seem to be comprehensive, or correlate sufficiently with clinically relevant outcomes for general uptake. In an attempt to provide direction for the future development of a new endometriosis classification system that is clinically relevant, three essential projects were defined: to review existing classification and staging systems for endometriosis; to develop a standard glossary to be utilized across the field of endometriosis; and to assess the current knowledge and uptake of classification systems among practitioners in the field. In the first project, 22 published classification and staging systems for endometriosis were summarized as well as the studies evaluating these with regards to feasibility, validity and reproducibility ( International Working Group of AAGL, ESGE, ESHRE and WES et al. , 2021d , e , f ). The second project resulted in the publication of a terminology for endometriosis ( International Working Group of AAGL, ESGE, ESHRE and WES et al. , 2021a , b , c ). For the third project, considering the uptake of the different classification systems, we conducted a survey to find out whether clinicians were routinely using any classification for endometriosis in clinical practice, which system is used most frequently, and what the motivations of clinicians are to use, or not use, any classification in endometriosis. The current paper reports the results of the survey. Of particular focus were the three systems most commonly used: the Revised American Society for Reproductive Medicine (rASRM) classification ( American Society for Reproductive Medicine, 1997 ), the endometriosis fertility index (EFI) ( Adamson and Pasta, 2010 ) and the ENZIAN classification ( Tuttlies et al ., 2005 ). With regards to the ENZIAN classification, a revised version of the classification, #ENZIAN ( Keckstein et al. , 2021 ), has meanwhile been published, but this was not available and hence not considered when the survey was conducted.

Of the 1251 respondents to the survey, the majority represented Europe (40.8%) and North-America (28.8%) ( Fig. 1 ). Figure 2 shows the frequencies of the profession of the respondents. For the final analysis, responders were restricted to practicing clinicians, which included non-gynaecologist surgeons and gynaecologist-surgeon (‘–surgeon’), and gynaecologists not performing surgery, reproductive endocrinologists, fertility specialists and sonographers (‘non-surgeon’). From these groups, nine respondents were excluded as they reported they did not manage women with endometriosis in their clinical practice. The final dataset included 1178 respondents. One-third of these reported managing less than 10 endometriosis patients per month, and this proportion did not differ between the surgeon and non-surgeon groups. Within the surgeon group, 85% reported performing more than five endometriosis surgeries per month ( Fig. 2 ). Overview of replies to the survey on endometriosis classification systems, across different regions. Overview of professions and expertise of the respondents. The rASRM classification system was the best known and most frequently used system, with only 4.7% of the respondents indicating they did not know or use the system. The EFI system and ENZIAN system were known by 76.1% and 53.8% of respondents, respectively, but used by only a minority (27.3% for EFI, 17.6% for ENZIAN) ( Fig. 3 ). Knowledge and use of ENZIAN, rASRM and EFI. rASRM, Revised American Society for Reproductive Medicine; EFI, Endometriosis Fertility Index. Overall, 75.5% of the respondents indicated that they currently use a classification system for endometriosis. One-third of the respondents further reported that they use more than one system (26.6% uses two systems, 8.1% uses three or more systems). The rASRM system was most often used. A minority of respondents (3.7%, n = 37) indicated that they use another published classification system (not ENZIAN, rARSM or EFI) or their own system ( Fig. 4 ). Current use of a classification system, and which system is used. On the question of which problems responders had encountered with the existing classification systems, 22.7% replied that they do not encounter any problems. The remaining respondents indicated a variety of problems. The lack of clinical relevance (n = 341) was most often selected ( Fig. 5 ). Problems with use of the existing classification systems and reasons for not using a classification system. The vast majority of respondents (95.1%) replied positively to the question on whether they would use a simple surgical descriptive system for endometriosis, if available ( Fig. 6 ). They indicated that standardization of reporting and prediction of response to treatment would be the main motivating factors to do so. Of the 4.9% of respondents not motivated to use a new system, some explained they were happy with the existing systems, while others considered that classification in endometriosis was not needed or impossible. The rest of respondents would use the system if it included patient symptoms, was clinically relevant and/or complete. Interest in a new simple surgical descriptive system for endometriosis. The responses were compared between those respondents that indicated surgeon (non-gynaecologist) or gynaecologist-surgeon as their profession, and other clinicians (gynaecologists not performing surgery, reproductive endocrinologists, fertility specialists, sonographers) ( Table I ). There were no clear differences between surgeons and non-surgeons with regards to the knowledge and use of any classification systems, although surgeons more often reported using the ENZIAN classification (25.5% versus 7.7%, P = 0.00001). With regards to the reasons for not using a classification system, surgeons more often indicated the lack of clinical relevance compared to non-surgeons (75.0% versus 51.7%, P = 0.00058). With regards to a new descriptive system, surgeons more frequently reported the following motivations, compared to non-surgeons: to predict complexity to assist in surgical planning (50.4% versus 25.0%, P  < 0.00001), billing purposes (15.8% versus 5.2%, P = 0.000017), standardization of reporting (79.6% versus 68.5%, P = 0.00026) and research purposes (42.9% versus 34.3%, P = 0.014). Comparison of the replies of surgeons versus non-surgeons to questions in a survey on use of endometriosis classification systems. Non-gynaecologist and gynaecologist surgeons. Gynaecologists not performing surgery, reproductive endocrinologists, fertility specialists, sonographers. Significant ( P  < 0.05) in comparing surgeons versus non-surgeons. rASRM, Revised American Society for Reproductive Medicine. In the comparison by continent, there was significant variation in the frequency of professions of the respondents and consequently in the number of surgeries they performed ( Table II ), but the level of expertise with endometriosis (i.e. the number of patients seen in clinical practice) was similar. Across continents, between 73.5% and 80.4% of respondents stated they currently use a classification system. There was lower knowledge and use in North-America, as compared to the rest of the world concerning ENZIAN (32.0% versus 62.1%, P  < 0.00001) and EFI (60.5% versus 82.0%, P  < 0.00001). With regards to the primary motivation to use a descriptive system, standardization was most often selected in all continents, apart from Asia and South-America, where prediction of response to treatment was the primary motivation. These results, specifically for Oceania and Africa, should be considered with caution considering the low number of replies from these areas. Comparison of replies to the survey by continent.

A cross-sectional study was conducted using an online survey, which focused on classification of endometriosis. The questions were drafted by an international group of experts in endometriosis representing four societies: the American Association of Gynecologic Laparoscopists (AAGL), European Society for Gynaecological Endoscopy (ESGE), ESHRE and the World Endometriosis Society (WES). The survey was conducted online and afterwards distributed amongst all members of the participating societies and the members of the American Society for Reproductive Medicine (ASRM). The survey included 11 questions organized in three sections. The first section focused on the participants’ background and included questions related to their country, professional status (profession, experience) and expertise in managing endometriosis patients ( Supplementary Data 1 ). The second part of the survey focused on existing classification systems, and the third part on the uptake of a potential new descriptive system for endometriosis. The survey was open between 15 May and 1 July 2020. Recruitment strategies included mass mailings by each of the participating societies and promotion on social media. A total of 1251 replies were received. The results of the survey were exported to SPSS 19 (IBM Corp., Armonk, NY, USA) for Windows for further analysis. Analysis and comparisons were focused on respondents who treat patients with endometriosis in clinical practice. Two sub-analyses were conducted, comparing surgeons versus other physicians, and replies between different regions. Statistically significant differences ( P  < 0.05) were assessed through Chi-square analysis.

This report summarizes the replies of 1178 clinicians, including surgeons, gynaecologists, reproductive endocrinologists, fertility specialists and sonographers, all managing women with endometriosis in their clinical practice. Questions focused on the current use of endometriosis classification systems, problems encountered and interest in a new simple surgical descriptive system for endometriosis. Overall, three-quarters of the respondents indicate that they use a classification system for endometriosis, with limited variation according to profession or location. The rASRM classification system, the oldest system, was the best known and used. The ENZIAN classification system, published in 2005, and the EFI system, published in 2010, were known by half of the respondents, but used less often, by one in five and one in four clinicians, respectively. The ENZIAN classification system was more often used by surgeons. Our results highlight some problems with the currently available classification systems. The most often reported problem, both by physicians using a classification system and those that do not, is the lack of clinical relevance. The complexity of the currently available classification systems is also considered a barrier for uptake, which is in line with previous reports ( Adamson, 2011 ; Johnson et al. , 2017 ). It should be noted, in this respect, that the results of the present survey reflect the ENZIAN classification, and can not necessarily be extrapolated to the revised version of the classification, #ENZIAN ( Keckstein et al. , 2021 ). In contrast to the high uptake of the rASRM, ENZIAN and EFI systems, the vast majority of clinicians managing endometriosis intended to use a new simple surgical descriptive system for endometriosis if developed. Standardization of reporting and prediction of response to treatment would be the main motivating factors to do so: the latter is consistent with the lack of clinical relevance of the current available systems. Standardized reporting of surgical findings is implemented in the WERF EPHect ( Becker et al. , 2014 ) and CORDES ( Vanhie et al. , 2016 ) questionnaires, which are currently tools for research purposes and not intended for clinical reporting. Any new clinically relevant classification system would need to be designed based on robust data analysis, by a multidisciplinary team, including experts in classification system development and validated across settings for its intended utility. Currently, the EFI is the only classification for which such testing was conducted in multiple studies in different countries. It is vital that both design and validation studies of any new tool would require robust assessment of metrics such as association with patient outcomes, including prediction of response to treatment, if the tool is intended for this clinical purpose. A standardized reporting system and anatomical classification of the endometriosis findings is a necessity for the further development of a grading system for clinical prediction. Although confined to the inherent limits of the methodology, this report provides relevant information with regards to the uptake of currently available systems and suggests that clinicians worldwide are open to using a new classification system for endometriosis that can achieve standardized reporting, and is clinically relevant and simple. These considerations should be taken into account in the development of future endometriosis classifications.

Supplementary data are available at Human Reproduction Open online.

All data are incorporated into the article and its online supplementary material .

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