{"paper_id":"2e538734-7b09-4065-9018-2d1267bf7873","body_text":"Othman et al. \nMiddle East Fertility Society Journal           (2024) 29:10  \nhttps://doi.org/10.1186/s43043-024-00169-7\nRESEARCH\nDiagnostic delay and health-related quality \nof life in Egyptian women with endometriosis\nEssam R. Othman1,2,3*†  , Ahmed M. Abdelmagied1†, Maha Y. Khashbah1,2, Cornelis B. Lambalk3 and \nVelja Mijatovic3 \nAbstract \nBackground Firstly, to measure indicators of health-related quality of life (HRQoL) in Egyptian women with endome-\ntriosis; and secondly, to estimate time interval from start of symptoms until endometriosis diagnosis is made (diagnos-\ntic delay) in Egyptian women with the disease.\nMaterial and methods Before laparoscopy for pelvic pain and/or infertility, eligible Egyptian women completed \nGlobal Study of Women’s Health (GSWH) questionnaire and validated Arabic version of Rand SF 36 (SF-36). Accord-\ning to laparoscopic findings, participants were divided to endometriosis group and control women with no pelvic \nabnormalities.\nResults Seventy women with endometriosis and 57 symptomatic controls without endometriosis were enrolled. \nA diagnostic delay of 36 months (IQR 22.5–60) was observed in women with endometriosis while symptomatic \ncontrols had a delay of 48 months (IQR 24–84). The difference was not statistically significant (P = 0.08). Bodily pain \n(BP) scores were significantly lower in women with endometriosis than controls [80.0 (45.0–100.0) versus 100.0 \n(68.75–100.0) respectively, P is 0.01]. Women with advanced endometriosis had significantly lower scores for physical \nfunctioning (PF), role limitation due to physical function (RP), and BP compared to women with mild endometriosis, \nand to controls. Physical component summary (PCS) scores were significantly lower in women with advanced stage \nendometriosis [41.51 (34.19–51.54] compared to women with early-stage disease [58.33 (50.98–60.37)] or control \ngroup [54.72 (48.81–59.58)]. Patient’s age, intensity of noncyclical pelvic pain, and disease stage are determining fac-\ntors of HRQoL in women with endometriosis.\nConclusions Egyptian women with endometriosis experience relatively short diagnostic delay, poor bodily pain \nscores, and impaired physical health for which age, disease stage, and non-cyclic pain are determinants. Multi-discipli-\nnary endometriosis centers, educational programs, and patient support groups are needed in Egypt.\nKeywords Quality of life, Diagnostic delay, Endometriosis, Egypt\nOpen Access\n© The Author(s) 2024. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which \npermits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the \noriginal author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or \nother third party material in this article are included in the article’s Creative Commons licence, unless indicated otherwise in a credit line \nto the material. If material is not included in the article’s Creative Commons licence and your intended use is not permitted by statutory \nregulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this \nlicence, visit http://creativecommons.org/licenses/by/4.0/.\nMiddle East Fertility\nSociety Journal\n†Essam R. Othman and Ahmed M. Abdelmagied contributed equally to this \nwork.\n*Correspondence:\nEssam R. Othman\nessamothman@aun.edu.eg\nFull list of author information is available at the end of the article\n\nPage 2 of 9Othman et al. Middle East Fertility Society Journal           (2024) 29:10 \nBackground\nEndometriosis is a menstrual cycle dependent, chronic, \ninflammatory, systemic disease that presents primarily \nwith pelvic pain. It affects 2–10% of women of reproduc -\ntive age leading to variable forms of pelvic pain, and sub -\nfertility [1]. Because of the heterogeneity of symptoms, \nand invasiveness of the diagnostic modality, i.e., lapa -\nroscopy, women with endometriosis experience a vari -\nable diagnostic delay [2]. During this time, women with \nendometriosis lose days at college and/or work, suffer \nfrom lowered self-esteem, have disturbed relationships, \nand often feel their pains will never disappear, which may \nerode their confidence in their physicians. These effects \nnegatively impact women’s productivity, professional per-\nspectives, emotional wellbeing, and social lives [3].\nHealth-related quality of life (HRQoL) encompasses \nphysical health, mental state, and social wellbeing in rela-\ntion to a disease or its treatment [4]. Endometriosis has \nbeen shown in several studies to impair nearly all aspects \nof HRQoL in affected women [4, 5]. However, some of the \nprevious studies suffered important limitations includ -\ning not using a validated HRQoL tool, an inadequately \nselected control group, not considering diagnostic delay \nand disease stage as factors affecting HRQoL, and focus -\ning mainly on Western populations.\nWomen perceive menstruation, menstrual problems, \nand endometriosis symptoms in a way specific to their \nculture, values, and beliefs. Arab women with endome -\ntriosis showed lower mental and physical health com -\nponents compared to women in other communities [6]. \nIn a conservative society like Egypt, menstruation and \nrelated events represent a taboo enveloped by a culture \nof secrecy [7]. Similarly, infertile women are often stig -\nmatized by their family/ community [8]. Despite having \na special cultural background, Egyptian women, particu -\nlarly those in the more conservative community of the \nsouth, were underrepresented in studies investigating \neffect of endometriosis on HRQoL.\nTherefore, in the current study, conducted in the south \nof Egypt, we measure different domains of HRQoL in \nEgyptian women with endometriosis using a validated \nArabic version of SF-36. We also assess determinant fac -\ntors of HRQoL in these women. In addition, we evaluate \nthe diagnostic delay experienced by Egyptian Women \nwith endometriosis.\nMaterial and methods\nThe present study was part of a larger research pro -\nject, funded by Science and Technology Development \nFund (STDF), Egyptian Ministry of Higher Education, \nparts of which have already been published [9, 10]. We \nrecruited 70 women with endometriosis (39 women with \nearly-stage endometriosis, and 31 women with advanced \nstage disease) and 57 symptomatic controls without \nendometriosis in the period from December 2014 to May \n2016.\nStudy design and settings\nThis cross-sectional survey was conducted at the Wom -\nen’s Health Hospital, University of Assiut, in the South of \nEgypt.\nStudy participants\nReproductive age women (18–45  years) scheduled for \nlaparoscopy to investigate their pelvic pain and/or infer -\ntility, were asked to participate in the study. Exclusion \ncriteria were prior endometriosis diagnosis (whether \nconfirmed with surgery or imaging), pelvic pathology \nother than endometriosis, hormonal treatment within \nthe last 3 months, or pregnancy/lactation in the previous \n6 months before surgery.\nSample size calculation\nEndometriosis is commonly associated with various \nforms of chronic pelvic pains (dysmenorrhea, dys -\npareunia, non-cyclic pelvic pain, cyclic dyschezia and \ndysuria). In addition, women with endometriosis have \nhigher risk of multi-site pain co-morbidities (fibromyal -\ngia, migraines, rheumatoid arthritis, and osteoarthritis). \nMoreover, bladder pain syndrome/interstitial cystitis \nand irritable bowel syndrome are commonly co-occur -\nring with endometriosis [11]. We assumed that women \nwith endometriosis may have higher impairment in the \ndomain of bodily pain compared to even the sympto -\nmatic controls.\nAccording to the SF-36 manual and interpretation \nguide [12], detecting a 10-point difference in bodily \npain between women with endometriosis and controls \nrequires 71 cases per group, at a two tailed alpha of 0.05 \nand power of 80%.\nEthical approval\nThe research protocol was approved by the Science and \nTechnology Development Fund (STDF), which is a part \nof the Egyptian Ministry of Higher Education in 2014. \nAdditional approval was obtained by The Institutional \nReview Board at the Faculty of Medicine, University of \nAssiut, (IRB# 17,400,008) in February 2018 to use the \ndata for publication.\nInformed consent\nA research team member (MYK) explained the study in \ndetails and its objectives to the participants and obtained \ntheir verbal informed consent to take part in the study. \nAnother researcher (ERO) assured participants about \n\nPage 3 of 9\nOthman et al. Middle East Fertility Society Journal           (2024) 29:10 \n \ndata anonymity to protect the confidentiality of their \ninformation and double checked that participants gave \ntheir verbal informed consent.\nInterview\nEarly in the morning, on the day of laparoscopy, par -\nticipants were interviewed by a member of the research \nteam to complete two questionnaires: Global Study of \nWomen’s Health questionnaire (GSWH) [3], which was \ncompleted by the researcher interviewing the patient, \nand the validated Arabic version of Rand SF-36 ques -\ntionnaire [13], which was completed by the patient her -\nself if literate enough. Otherwise, the researcher read \nand explained questions to the patient and recorded her \nresponses after read-back.\nQuestionnaires\n– Global Study of Women’s Health (GSWH) question-\nnaire: which is a 67-item questionnaire on present -\ning symptoms, physical functioning, medical, and \nreproductive history, time since start of symptoms \nand health resource use [3]. The GSWH question -\nnaire incorporates questions and instruments previ -\nously validated for women with pelvic pains or other \nsymptom groups. These include Short Version-36 \nV2 (SF-36 v2), The Work Productivity and activity \nImpairment (WPAI) questionnaire, the IRB Rome \nIII questionnaire to assess pelvic pain due to irritable \nbowel and standardized pelvic pain symptom assess -\nment used in previous studies in Oxford [14].\n– Short version-36 (SF-36) is a tool used to assess gen -\neral health related quality of life. Arabic translation of \nthis questionnaire is available that has already been \nvalidated [13]. Other disease-specific questionnaires \nlike Endometriosis Health Profile-30 (EP-30) and \nEndometriosis Health Profile-5 (EP-5) have not been \ntranslated to Arabic Language. The  SF-36 question -\nnaire consists of 36 questions that are grouped into 8 \nmain domains over the last four weeks. These include \nPhysical functioning (FP; 10 items), Role limitation \ndue to physical function (RP; 4 items), Role limitation \ndue to emotional factors (RE; 3 items), Vitality (VT; \n4 items), Mental Health (MH; 5 items), Social Func -\ntioning (SF; 2 items), Bodily Pain (BP; 2 items), Gen -\neral Health (GH; 5 items), and perception of health \nin comparison to the last year (1 item). Each item \nresponse is given a raw score based on SF-36 manual. \nRaw scores are then summated to give domain scores \nranging from 0 to 100 where 0 means lowest quality \nof life and 100 indicates best quality of life. In addi -\ntion, the 8 domain scores are combined to produce \nphysical component summary (PCS) score (derived \nfrom PF, RP , BP , GH), and mental component sum -\nmary (MCS) score (derived from RE, MH, SF, VT) \n[12, 13]. All psychometric measures of SF-36 valida -\ntion are available in the SF 36 Health Survey: Manual \nand Interpretation Guide [12].\nUsing the GSWH questionnaire allowed us to sys -\ntematically capture the demographic and clinical char -\nacteristics of study participants; including structured \nmenstrual/reproductive history, detailed symptoms, and \nthe diagnostic delay. Adding SF-36 questionnaire permit-\nted the measure of different domains of the participants’ \nHR-QoL which were ultimately summated into PCS and \nthe MCS scores.\n– Calculation of the diagnostic delay: Women were \nasked to self-report the earliest age at which they \nexperienced endometriosis-related symptoms (infer -\ntility or various forms of pelvic pain). Time interval \nthat lapsed between age at onset of symptoms and \nage at which endometriosis was surgically diagnosed \nrepresented the actual diagnostic delay [3, 6].\nSurgical diagnosis of endometriosis\nEndometriosis was diagnosed during laparoscopy \naccording to typical morphologic features of the lesions. \nWomen whose laparoscopic examination revealed a nor -\nmal pelvis were classified as idiopathic infertility/pelvic \npain and served as the control group. Laparoscopies were \nperformed in the proliferative phase of the menstrual \ncycle by experienced surgeons. During surgery, endo -\nmetriosis was scored according to the revised American \nSociety of Reproductive Medicine (ASRM) scoring sys -\ntem. Endometriosis was rated as either minimal (stage I), \nmild (stage II), moderate (stage III), or severe (stage IV). \nMenstrual dates were assessed based on patient’s men -\nstrual history.\nStatistical methods\nAll statistical analysis in the current study was done \nusing Social Package of Social Scientists (SPSS), ver -\nsion 21 (IBM Corp, Armonk, NY, USA) statistical soft -\nware. Kolmogorov-Smirnov test and the Shapiro-Wilk \ntest were used to examine the distribution of data. \nClinical and demographic data were expressed as mean \n± standard deviation (SD) except for number of liv -\ning children, duration of infertility, Numerical Rating \nScore (NRS) for dysmenorrhea, deep dyspareunia, and \nnon-cyclic pelvic pain, and diagnostic delay in which \ndata were expressed as median and interquartile range \n(IQR). SF-36 domain scores in women with endome -\ntriosis and controls were not normally distributed, so, \n\nPage 4 of 9Othman et al. Middle East Fertility Society Journal           (2024) 29:10 \nnon-parametric statistics were used, and scores were \nexpressed as median ± IQR. Mann-Whitney U test \nwas used to compare women with endometriosis ver -\nsus symptomatic controls. Kruskal-Wallis test was used \nto compare scores across early-stage endometriosis, \nadvanced stage endometriosis, and symptomatic con -\ntrols. Pairwise comparisons among the 3 groups were \ndone with Mann-Whitney U  test and Bonferroni cor -\nrection. Statistical significance was considered if P \nvalue ≤ 0.05. To identify determinants that are asso -\nciated with low PCS, and MCS in women with endo -\nmetriosis, a multiple logistic regression model was \ndeveloped in which both component summary scores \nwere dichotomized; either below or above their respec -\ntive median value (given score 1 or 0, respectively), and \nconsidered as the dependent variable. Clinical factors \n(age, BMI, parity, time since start of symptoms, endo -\nmetriosis stage, numerical rating scale (NRS) for dys -\nmenorrhea, dyspareunia, and non-cyclic pelvic pain) \nwere incorporated in the model as independent vari -\nables [15].\nResults\n1. Patients’ characteristics and results of clinical/sur -\ngical evaluation of recruited women are shown in \nTables 1 and 2 respectively.\n2. Diagnostic delay experienced by Egyptian women \nwith endometriosis:\n A diagnostic delay of 36 months (IQR 22.5–60) was \nobserved in women with endometriosis while symp -\ntomatic controls had a delay of 48  months (IQR \n24–84). The difference was not statistically significant \n(P = 0.08), as seen in Table 2. Women complaining of \ninfertility represented 44.3% of endometriosis group, \nand 87.7% of symptomatic control women.\n3. SF-36 domain scores in women with endometriosis \nand symptomatic controls:\nTable 1 Characteristics of study participants\nItem Endometriosis N = 70 Control women N = 57 P value\nDemographics\n Age (years) 28.56 ± 5.72 28.96 ± 5.7 0.690\n BMI (kg/m2) 25.32 ± 4.5 27.34 ± 4.29 0.011\n Urban (N, %) 9 (12.9%) 7 (12.3%) 0.922\n Rural (N, %) 61 (87.1%) 50 (87.7%)\n Number of living children 0.0 (0.0–1.0) 0.0 (0.0–0.0) 0.047\nMarital status\n Currently married 65 56 0.185\n Virgin 4 0\n Divorced/separated 1 1\nIndication of surgery (N, %)\n Infertility 31 (44.3%) 50 (87.7%) < 0.001\n Pelvic pain 16 (23.0%) 6 (10.5%)\n Infertility + Pelvic pain 11(15.7%) 1 (1.8%)\n Ovarian cysts (N, %) 5 (7.1%) 0\n Others (N, %t) 7 (10%) 0\n Duration of infertility (years) 3.0 (0.0–5.0) 4.0 (2.0–7.0) 0.048\nMenstrual days (N, %)\n < 2 days 0 1 (1.8%) 0.532\n 2–7 days 69 (98.5%) 55 (96.4%)\n > 7 days 1 (1.5%) 1 (1.8%)\nCycle length\n < 24 days 0 3 (5.3%) 0.068\n 24–35 days 62 (88.6%) 52 (91.2%)\n Infrequent (> 35 days) 7 (10%) 1 (1.8%)\n Too irregular (metrorrhagia) 1 (1.4%) 1 (1.8%)\n\nPage 5 of 9\nOthman et al. Middle East Fertility Society Journal           (2024) 29:10 \n \n As depicted in Table  3, women with endometrio -\nsis had significantly lower scores for the BP domain \nthan symptomatic controls [80.0 (45.0–100.0) versus \n100.0 (68.75–100.0) respectively, P is 0.01] indicating \npoorer quality of life in this domain. No statistically \nsignificant difference was detected between women \nwith endometriosis and symptomatic controls in \nother domains of the SF-36.\n4. SF-36 domain scores in women with endometriosis \nstratified by stage of the disease:\n A shown in Table 4, women with stages III/IV endo -\nmetriosis had significantly lower scores for PF [85.0 \n(50–100.0)] , RP [25.0 (0.0–75.0)], and BP [55.0 \n(35.0–85.0)], compared to women with stages I/II \ndisease [corresponding scores for PF, RP , and BP are: \n95.0 (85.0–100.0), 100.0 (25.0.0–100.0), and 100.0 \n(70.0–100.0), respectively] and to control women \n(corresponding scores are: 95.0 (82–100.0), 100.0 \n(0.0–100.0), and 100.0 (68.7–100.0), respectively). \nFor the domain of GH, women with stages III/IV \nendometriosis scored significantly less than women \nwith stages I/II disease [60.0 (45.0–85.0) versus 85.0 \n(70.0–90.0) respectively, P is 0.001).\n5. Physical component summary (PCS) and mental \ncomponent summary (MCS):\n PCS and MCS for women with endometriosis and \nsymptomatic controls were calculated according to \nthe SF-36 manual [12]. These are standardized com -\nbined scores with a mean of 50, and standard devia -\ntion of 10. According to our results, neither PCS nor \nMCS differed significantly between women with \nendometriosis and controls (Table 3). Breaking down \nendometriosis group by disease stage showed that \nwomen with stages III/IV endometriosis had signifi -\ncantly lower PCS scores compared to women with \nstages I/II disease or control group (Table  4). On the \nother hand, there was no significant difference in \nMCS scores between different stages of endometrio -\nsis or control women (Table 4).\n6. Determinants of low PCS and MCS scores in women \nwith endometriosis:\nTable 2 Clinical/surgical evaluation and diagnostic delay in study participants\nNAS numerical analogue scale\nEndometriosis (N = 70) Controls (N = 57) P value\nIntensity of pelvic pain (NAS)\n Dysmenorrhea 7.0 (0.0–9.0) 0.0 (0.0–5.0) 0.001\n Dyspareunia 2.0 (0.0–6.5) 0.0 (0.0–5.0) 0.214\n Non-cyclic pain 0.0 (0.0–6.0) 0.0 (0.0–6.0) 0.312\nEndometriosis stage: (N, percent)\n Stages I/II endometriosis 39 (56%) N/A\nStages III/IV endometriosis 31 (44%) N/A\nDiagnostic delay: (months since start of symptoms)\n Diagnostic delay (in months; median and IQR) 36 (22.5–60) 48 (24–84) 0.080\nTable 3 SF-36 domain scores in women with endometriosis patients and controls. Data expressed as median and interquartile range \n(IQR)\nSF-36 items Endometriosis (N = 70) Controls (N = 57) P value\nPhysical Functioning (PF) 95.0 (73.75–100.0) 95.5 (82.0–100.0) 0.366\nRole limitation due to physical function (RP) 62.5 (0.0–100.0) 100.0 (0.0–100.0) 0.261\nRole limitation due to emotional factors (RE) 66.7 (0.0–100.0) 66.7 (0.0–100.0) 0.722\nVitality (VT) 70.0 (50.0–85.0) 70.0 (50.0–82.5) 0.850\nMental Health (MH) 62.0 (40.0–76.0) 60.0 (40.0–76.0) 0.894\nSocial Functioning (SF) 50.0 (50.0–50.0) 50.0 (50.0–62.0) 0.265\nBodily Pain (BP) 80.0 (45.0–100.0) 100.0 (68.75–100.0) 0.016\nGeneral Health (GH) 75.0 (60.0–86.25) 75.0 (55.0–90.0) 0.739\nPhysical Component Summary (PCS) 51.7 (41.34–58.99) 54.73 (48.81–59.58) 0.088\nMental Component Summary (MCS) 42.05 (30.58–48.63) 38.82 (29.47–46.03) 0.529\n\nPage 6 of 9Othman et al. Middle East Fertility Society Journal           (2024) 29:10 \n A multi-logistic regression model was developed \nwith PCS/ MCS scores are the dependent variables \n(dichotomized, with score below and above their \nrespective median given the code 1 and 0, respec -\ntively), and participants’ demographic/clinical factors \nas the independent variables. Our model has shown \nthat age (OR: 1.22, CI: 1.01–1.49, P value: 0.036), NRS \nfor non-cyclic pelvic pain (OR: 1.93, CI: 1.27–2.95, P \nvalue: 0.002), and advanced stage endometriosis (OR: \n28.9, CI: 3.9–218.09, P value: 0.001) are associated \nwith low PCS scores in women with endometriosis. \nNo specific determinants were significantly associ -\nated with low MCS scores in the group of women \nwith endometriosis (Table 5).\nDiscussion\nOur results show that Egyptian women with endome -\ntriosis experienced a relatively short diagnostic delay and \nhad poorer bodily pain scores compared to symptomatic \ncontrols. Patient’s age, intensity of non-cyclic pelvic pain, \nand advanced disease stage are determining factors of \nphysical health in Egyptian endometriosis patients.\nEgyptian women were underrepresented in previous \nresearch on endometriosis-related HRQoL. SF-36, which \nperforms well in evaluation of HRQoL in endometriosis, \nTable 4 SF-36 domain scores in early (stages I/II) and advanced (stages III/IV) endometriosis. Data expressed as median and \ninterquartile range (IQR)\nSF-36 items Mild Endometriosis \n(Stages I and II) \nN = 39\nAdvanced endometriosis \n(Stages III and IV) N = 31\nControl women N = 57 P value\nMild endo. \nvs. control\nMild vs. \nsevere \nendo\nSevere \nendo. vs. \ncontrol\nPhysical Functioning (PF) 95.0 (85.0–100.0) 85.0 (50–100.0) 95.0 (82–100.0) 1.00 0.020 0.056\nRole limitation due to physical \nfunction (RP)\n100.0 (25.0.0–100.0) 25.0 (0.0–75) 100.0 (0.0–100.0) 1.00 0.002 0.011\nRole limitation due to emo-\ntional factors (RE)\n100.0 (0.0–100.0) 33.3 (0.0–100.0) 66.6 (0.0–100.0) 0.32\nVitality (VT) 70 (55.0–90.0) 65.0 (50.0–80.0) 70.0 (50.0–82.5) 0.48\nMental Health (MH) 60.0 (40.0–76.0) 64.0 (36.0–76.0) 60.0 (40.0–76.0) 0.98\nSocial Functioning (SF) 50.0 (50.0–50.0) 50.0 (37.5–50.0) 50.0 (50.0–62.5) 0.24\nBodily Pain (BP) 100.0 (70.0–100.0) 55.0 (35.0–85.0) 100.0 (68.7–100.0) 1.00 < 0.001 < 0.001\nGeneral Health (GH) 85.5 (70.0–90.0) 60.0 (45.0–85.0) 75.0 (55.0–90.0) 0.145 0.003 0.260\nPhysical Component Summary \n(PCS)\n58.33 (50.98–60.38) 51.52 (34.20–51.54) 54.73 (48.81–59.59) 0.868 < 0.001 < 0.001\nMental Component Summary \n(MCS)\n37.8 (29.49–49.20) 43.3 (32.93–47.01) 38.82 (29.47–46.03) 0.789\nTable 5 Multiple logistic regression analysis of PCS/ MCS scores (as dependent variables) and participants’ clinical/demographic \ncriteria (as independent variables) in Egyptian women with endometriosis\nNAS numerical analogue scale\nIndependent variable PCS MCS\nOdds ratio 95 Confidence \ninterval (CI)\nP value Odds ratio 95 Confidence \ninterval (CI)\nP value\nAge 1.22 1.01–1.49 0.036 1.15 0.92–1.11 0.744\nBMI 0.92 0.76–1.10 0.362 0.95 0.85–1.07 0.418\nTime since start of symptoms 0.98 0.96–1.009 0.240 0.98 0.97–1.005 0.180\nDysmenorrhea (NAS) 0.76 0.55–1.02 0.074 0.94 0.78–1.11 0.442\nDyspareunia (NAS) 1.12 0.85–1.47 0.391 1.10 0.92–1.32 0.291\nNon-cyclic pelvic pain (NAS) 1.93 1.27–2.95 0.002 1.16 0.96–1.39 0.112\nNumber of living children 1.31 0.63–2.74 0.464 0.83 0.50–1.36 0.466\nEndometriosis stage (stages III/IV \nversus stages I/II)\n28.9 3.9–218.09 0.001 0.62 0.21–1.82 0.384\n\nPage 7 of 9\nOthman et al. Middle East Fertility Society Journal           (2024) 29:10 \n \nwas used in this study [16]. We investigated factors like \npatient’s age, diagnostic delay, symptom severity, and dis-\nease stage for their influence on HRQoL. Using sympto -\nmatic controls likely has prevented overestimation of the \nnegative effect of endometriosis on HRQoL compared \nto if the control group had consisted of healthy asymp -\ntomatic women. A point of strength in our study is that \nall endometriosis cases and symptomatic controls were \nsurgically evaluated.\nA possible explanation of the occurrence of diagnos -\ntic delay in Egyptian women with endometriosis is the \ncommon culture of menstrual taboo, with subsequent \nnormalization of symptoms by families and society [7] as \nwell as limited availability of reproductive health educa -\ntion [17], particularly knowledge about endometriosis, \namong Egyptian females [18]. Therefore, educational \nprograms for adolescents about endometriosis as a part \nof the school curriculum [19], as well as incorporating \nthe disease into national clinical guidelines and fostering \nmulti-disciplinary collaborations in endometriosis care, \nmay lead to more awareness for endometriosis and may \nfavorably impact diagnostic delay [20].\nStudies addressing the length of the diagnostic delay in \nwomen with endometriosis have reported delays up to \nnearly 11 years which may vary among centers and coun -\ntries [3, 21–23].\nAs laparoscopy is highly subsidized (and consequently \naffordable) in Egyptian governmental hospitals, this may \nencourage gynecologists to order it early when inves -\ntigating infertility/pelvic pain as hallmarks of endome -\ntriosis. This practice may contribute to the relative short \ndelay in diagnosis of 36 months in Egyptian women with \nendometriosis when compared to studies in other coun -\ntries [3].\nThis is not in line with previous research which showed \nthat state-funded health care systems, compared to self-\nor insurance funded counterparts, usually results in \nlonger diagnostic delay [3].\nHowever, similar diagnostic delay, ranging between \n2 and 3.7 years, as found in our study, were reported in \nChinese, European, and American women [3, 24, 25].\nThe high prevalence of infertility in our cohort of \nwomen with endometriosis might have contributed to \nthe relatively short diagnostic delay. Prior studies showed \nthat the time to diagnosis is shorter in women with endo-\nmetriosis associated infertility compared to patients \nwith pain related symptoms for seeking medical help [2, \n25, 26]. Among general practitioners, this translates as \nthe sense of urgency to establish a timely diagnosis and \nto offer treatment of endometriosis in order to prevent \nfuture infertility [20].\nPrior studies conducted on different popula -\ntions showed that women with endometriosis have \nimpairments in different domains of SF-36 when com -\npared to symptomatic controls [3, 27]. In addition, Nnoa-\nham and coworkers found that women with moderate/\nadvanced stage endometriosis had significantly lower \nPCS scores than women with minimal/mild disease [3]. \nOur results support these findings.\nTwo other studies investigated Egyptian women with \nendometriosis. One study found that endometriosis \npatients with adhesions had lower HRQoL scores than \nendometriosis women lacking them [28]. This study \nincluded infertile women with stage III endometrio -\nsis only, with no control group, and the authors used \nthe Global Quality of Life scale, which is not validated \nfor endometriosis, and does not recognize domains of \nimpairment. The second study used SF-12, and EHP-5 to \nmeasure HRQoL in endometriosis patients. Again, the \nstudy was not controlled, the Arabic version of the EHP-5 \nused was not validated in an independent study, the \nEHP-5 results were reported only as percentages, without \nactual scores, and the SF-12 scores were not mentioned \n[29].\nMousa et al. [6] found that the collective PCS and MCS \nwere lower in Arab women with endometriosis compared \nto symptomatic and asymptomatic controls. Moreover, \nwomen with endometriosis suffered a diagnostic delay \nof 11.61 years [6]. Although we could not identify a sig -\nnificant difference in MCS scores between endometriosis \npatients and symptomatic controls, we showed that MCS \nscores in both groups were below the population average, \nwhich is similar to Mousa et al. ’s findings. We and Mousa \net al. used the normative value of the US population for \ncomparison due to lack of normative values of these \nscores in Egypt or the Middle East [6]. Our sample size \nwas much smaller than the Mousa et al. study; however, \nwe focused on more homogeneous population in terms of \nethnicity and cultural characteristics (Egyptian women), \nrather than different Arab nationalities. Furthermore, \nmost recruited women in Mousa et al. ’s study were edu-\ncated and employed (around 60%). In our study, 87% of \nwomen came from rural areas. Such women are generally \nless well educated or even illiterate and are housewives. \nThese differences in population characteristics may \naccount for the variability in findings. In addition, in the \nMousa et  al. ’s study, 67% of women with endometriosis \nhad chronic pelvic pain in comparison to only 23% in our \nstudy. This difference in clinical presentation might have \naffected care seeking behavior of women in that study. \nAs we depended in our study on participants’ recalling of \nwhen their symptoms started, it is also possible that the \nlower level of education in our participants might have \nincreased their recall bias [30].\nOur results showed that in Egyptian women with \nendometriosis, higher patient’s age was associated \n\nPage 8 of 9Othman et al. Middle East Fertility Society Journal           (2024) 29:10 \nwith lower PCS score of the SF-36 scale. Prior research \nshowed younger age was associated with poorer \ndomains in SF-36. However, the collective PCS and \nMCS scores were not reported or correlated to age [31].\nEndometriosis effects on HRQoL were not always \nrelated to disease stage [5 ]. However, our results, in \nagreement with Nnoaham and his group [3 ], showed \nadvanced stage disease to be significantly associated \nwith worse PCS scores in women with endometriosis. \nThe association of advanced stage endometriosis with \npoor physical health might be explained by the pres -\nence of variable degrees of symptom severity or associ -\nated comorbidities in advanced endometriosis patients \n[32].\nWe reported non-cyclic pelvic pain intensity as a sig -\nnificant determinant of low PCS scores in women with \nendometriosis. Prior research showed that dysmenorrhea \nand non-menstrual pain negatively impacted HRQoL \nin women with endometriosis [27]. On the other hand, \nreduction in dysmenorrhea and non-menstrual pelvic \npain using elagolix improved HRQoL and work produc -\ntivity in women with endometriosis pelvic pain [33].\nOur study is not without limitations. Our sample size \nwas modest, as we could recruit 90% of the required \nsample size as per the SF-36 Health Survey: Manual and \nInterpretation Guide [12]. We did not include a control \ngroup of healthy asymptomatic women. We could not \nclassify participants in our study according to their clini -\ncal presentation of pelvic pain or infertility due to the \nsmall number of pelvic pain cases in our endometriosis \n(N = 16) and the symptomatic control (N = 6) groups. \nFurthermore, a commonly cited disadvantage in obser -\nvational studies from a methodological point of view is \nthe potential for recall bias as the data are collected ret -\nrospectively. This represents an important limitation \nfor evaluating the diagnostic delay in our study as we \ndepended on patients memorizing when symptoms first \nstarted. Therefore, a longitudinal cohort study would \nbe more suited to investigate the associations between \nHRQoL and endometriosis. Finally, we could not evaluate \ndiagnostic delay separately at the level of general practi -\ntioner or gynecologist as the Egyptian health care system \nallows for patient self-selection of her health care pro -\nvider [34].\nIn conclusion: our study has shown that Egyptian \nwomen with endometriosis experience diagnostic delay \nand exhibit impaired physical health scores for which \npatient’s age, disease stage, and non-cyclic pain are sig -\nnificant determining factors. Multidisciplinary endome -\ntriosis care centers are needed in Egypt, together with \neducational programs to increase awareness about the \ndisease. Patient support groups are important require -\nment to empower endometriosis patients in Egypt.\nAcknowledgements\nThe authors would like to acknowledge all the nursing team in the laparos-\ncopy unit at University of Assiut, Women’s Hospital for helping with recruiting \ncases to the study. The authors would like to thank Dr. Ghada A Mahfouz, Fac-\nulty of Nursing, University of Assiut for providing the Arabic version of SF-36.\nAuthors’ contributions\nERO: conception of the idea, data collection, data analysis, manuscript \nwriting. AMA: data analysis, manuscript writing. MYK: data collection, data \nanalysis. CBL: data analysis, reviewing manuscript. VM: data analysis, reviewing \nmanuscript.\nFunding\nThe study was supported by a grant from Science and Technology Develop-\nment Fund (STDF), Egypt to E.R. O. grant ID# 5525.\nAvailability of data and materials\nThe dataset used for the development of this manuscript is available from the \nauthors upon request.\nDeclarations\nEthics approval and consent to participate\nThe research protocol was approved by the Science and Technology \nDevelopment Fund (STDF), which is a part of the Egyptian Ministry of Higher \nEducation in 2014. Additional approval was obtained by The Institutional \nReview Board at the Faculty of Medicine, University of Assiut, (IRB# 17400008) \nin February 2018 to use the data for publication.\nA research team member (MYK) explained the study in details and its objec-\ntives to the participants and obtained their verbal informed consent to take \npart in the study. Another researcher (ERO) assured participants about data \nanonymity to protect the confidentiality of their information and double \nchecked that participants gave their verbal informed consent.\nConsent for publication\nThe manuscript does not contain any individual person data. So, consent for \npublication is not applicable.\nCompeting interests\nThe authors declare no competing interests.\nAuthor details\n1 OB-GYN Department, University of Assiut, Assiut, Egypt. 2 Reproductive Sci-\nence Research Center, Assiut University, Assiut, Egypt. 3 Department of Repro-\nductive Medicine, Academic Endometriosis Center, Amsterdam University \nMedical Center, Vrije Universiteit Amsterdam, Amsterdam, The Netherlands. \nReceived: 10 October 2023   Accepted: 13 January 2024\nReferences\n 1. Becker CM, Bokor A, Heikinheimo O et al (2022) ESHRE guideline: endo-\nmetriosis. Hum Reprod Open 2022(2):hoac009\n 2. Arruda MS, Petta CA, Abrão MS, Benetti-Pinto CL (2003) Time elapsed \nfrom onset of symptoms to diagnosis of endometriosis in a cohort study \nof Brazilian women. Hum Reprod 18(4):756–759\n 3. Nnoaham KE, Hummelshoj L, Webster P et al (2011) Impact of endome-\ntriosis on quality of life and work productivity: a multicenter study across \nten countries. 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Pokrzywinski RM, Soliman AM, Chen J et al (2020) Achieving clinically \nmeaningful response in endometriosis pain symptoms is associated \nwith improvements in health-related quality of life and work productiv-\nity: analysis of 2 phase III clinical trials. Am J Obstet Gynecol 222(6):592.\ne1–592.e10\n 34. Muhammad YY, Nossier SA, El-Dawaiaty AA (2011) Prevalence and \ncharacteristics of chronic pelvic pain among women in Alexandria. Egypt \nJ Egypt Public Health Assoc 86(1–2):33–38\nPublisher’s Note\nSpringer Nature remains neutral with regard to jurisdictional claims in pub-\nlished maps and institutional affiliations.","source_license":"CC0","license_restricted":false}