{"paper_id":"750a120f-44ea-4915-b6d3-17a08d358cee","body_text":"Received\n 04/18/2023 \nReview began\n 04/28/2023 \nReview ended\n 05/02/2023 \nPublished\n 05/09/2023\n© Copyright \n2023\nWestwood et al. This is an open access\narticle distributed under the terms of the\nCreative Commons Attribution License CC-\nBY 4.0., which permits unrestricted use,\ndistribution, and reproduction in any\nmedium, provided the original author and\nsource are credited.\nDisparities in Women With Endometriosis\nRegarding Access to Care, Diagnosis, Treatment,\nand Management in the United States: A Scoping\nReview\nShannon \nWestwood \n \n, \nMackenzie Fannin \n \n, \nFadumo Ali \n \n, \nJustice Thigpen \n \n, \nRachel Tatro \n \n, \nAmanda\nHernandez \n \n, \nCadynce Peltzer \n \n, \nMariah Hildebrand \n \n, \nAlexnys Fernandez-Pacheco \n \n, \nJonathan R.\nRaymond-Lezman \n \n, \nRobin J. Jacobs \n1.\n Dr. Kiran C. Patel College of Osteopathic Medicine, Nova Southeastern University, Fort Lauderdale, USA\nCorresponding author: \nRobin J. Jacobs, \nrjacobs@nova.edu\nAbstract\nEndometriosis is a benign gynecological condition that elicits chronic pain in 2-10% of reproductive-age\nwomen in the United States and exists in approximately 50% of women with infertility. It creates\ncomplications such as hemorrhage and uterine rupture. Historically, the gynecologic symptoms of\nendometriosis have been associated with economic strain and inferior quality of life. It is suspected that\nendometriosis diagnosis and treatment are affected by health disparities throughout gynecological care. The\ngoal of this review was to collate and report the current evidence on potential healthcare disparities related\nto endometriosis diagnosis, treatment, and care across race, ethnicity, and socioeconomic status. This\nscoping review followed the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA)\nguidelines and searched the Excerpta Medica Database (EMBASE), Medline Ovid, Cumulated Index to\nNursing and Allied Health Literature (CINAHL), Web of Science, and PsycInfo databases for relevant articles\non the topic. Eligibility was established \na priori\n to include articles written in English, published between\n2015-2022, and reported on cohort, cross-sectional, or experimental studies conducted in the United States.\nInitially, 328 articles were found, and after screening and quality assessment, four articles were retained for\nthe final review. Results indicated that White women had higher rates of minimally invasive procedures\nversus open abdominal surgeries than non-White women. White women also had fewer surgical\ncomplications compared to all other races and ethnicities. Black women had higher rates of perioperative\ncomplications, higher mortality, and spent more time in the perioperative stage than any other race or\nethnicity. In the management of endometriosis, the limited research available showed that all non-White\nwomen encountered an increased risk of perioperative and postoperative complications compared to White\nwomen. More research is needed to explore diagnostic and treatment disparities beyond surgical\nmanagement, socioeconomic barriers, and improved representation of racial and ethnic minority women.\nCategories:\n Obstetrics/Gynecology, General Surgery, Public Health\nKeywords:\n surgical complication, women’s health, racial and ethnic disparities, general gynecology, gynecological\ndisorder\nIntroduction And Background\nEndometriosis is a chronic inflammatory disease that globally affects up to 10% of reproductive-aged\nwomen \n[1]\n. Defined as extra-uterine lesions composed of endometrial glands and stroma, the estrogen-\ndependent disease process is often associated with chronic pelvic pain, infertility, pregnancy complications,\nand a decreased quality of life \n[2,3,4,5,6]\n. Due to its dependence on ovarian cyclicity, endometriosis\ncommonly affects women between menarche and menopause \n[2,7]\n. Although clinically benign, the harmful\nimpacts on quality of life are significant. Pain and associated dysfunctions are detrimental to patients’\neconomic status and professional, educational, social, and family lives, proving endometriosis to be a\nsignificant medical, social, and economic issue \n[8,9]\n.\nWhile a clinical history of dyspareunia and dysmenorrhea may raise suspicions of endometriosis, the non-\nspecific nature of these symptoms is mimicked by several other potential etiologies. Additionally,\nendometriosis lacks pathognomonic features and biomarkers specific to the disease process \n[10]\n. Instead,\ndiagnosis relies upon surgical visualization and histological confirmation of extra-uterine lesions consisting\nof endometrial glands and stroma \n[11]\n. However, the presence of these lesions cannot exclude other\npotential etiologies for the patient’s symptoms, nor can the absence of lesions prevent endometriosis. The\nlack of sensitive, specific, non-invasive diagnostic methods contributes to a delay in the diagnosis of\nendometriosis that can last between four and eleven years, contributing to unnecessary, prolonged suffering\nand decreased quality of life in patients \n[10,12]\n.\nEndometriosis is a complex disease with a multifactorial etiology, and several theories surrounding its origin\nexist. The most widely accepted theory of what causes endometriosis is retrograde menstruation, where\n1\n1\n1\n1\n1\n1\n1\n1\n1\n1\n1\n \n Open Access Review\nArticle\n \nDOI:\n 10.7759/cureus.38765\nHow to cite this article\nWestwood S, Fannin M, Ali F, et al. (May 09, 2023) Disparities in Women With Endometriosis Regarding Access to Care, Diagnosis, Treatment,\nand Management in the United States: A Scoping Review. Cureus 15(5): e38765. \nDOI 10.7759/cureus.38765\n\nendometrial cells flow backward through the fallopian tubes. The cells move into the pelvic cavity, where\nthey can insert and grow. Cellular dysplasia of extra-uterine cells into endometrium-like cells has also been\nproposed, as has the theory that stem cells can give rise to the disease \n[13,14]\n. Other etiological factors may\ninclude altered or impaired immunity, complex hormonal influences and fluctuations, genetics, and\nenvironmental contaminants \n[15,16]\n.\nOn average, globally, it takes seven years to diagnose endometriosis after the onset of symptoms, causing\ndelays in diagnosis and subsequent treatment \n[17]\n. More than four million women of reproductive age have\nan endometriosis diagnosis in the United States; six out of ten cases go undiagnosed \n[12]\n. Historically,\nendometriosis was commonly known to affect White women while being seen as a “rare condition” for other\nraces, leading to misdiagnoses for chronic pelvic pain in non-Whites \n[18]\n. This review explored the literature\non endometriosis diagnosis, management, and treatment as it pertains to health inequities among women. \nReview\nMaterials and methods\nThis scoping review followed Preferred Reporting Items for Systematic Reviews and Meta-\nAnalyses (PRISMA) guidelines. Eligibility was established a priori to include articles written in English,\npublished between 2015-2022, and reported on cohort, cross-sectional, or experimental studies conducted\nin the United States. Initially, 328 articles were found, and after screening four were retained for the final\nreview. \nSearch Strategy \nThis scoping review searched Excerpta Medica Database (EMBASE), Medline Ovid, Cumulated Index to\nNursing and Allied Health Literature (CINAHL), Web of Science, and PsycInfo with completed searches on\nSeptember 26, 2022. The search strategy was created in EMBASE by the first author and reviewed by an\nexpert librarian. The goal of the search was to uncover what evidence is available on disparities in\nendometriosis care in the United States. The EMBASE search strategy was adapted for Medline Ovid,\nCINAHL, Web of Science, and PsycInfo. The search terms used were “endometriosis,” “endometrioma,”\n“social inequality,” “health care disparity,” “health care access,” “economic,” “income,” “gender,” “sexual,\nbias,” “disparities,” “minority,” and “poverty.” Multiple combinations of search terms were used to obtain\nmaximum results. The citations and bibliography sections of the included articles were reviewed; no articles\nwere found by other means (e.g., hand searching) that met the search criteria.\nThe four articles that met inclusion criteria were evaluated for method quality and the risk of bias using the\nJoanna Briggs Institute (JBI) critical appraisal tools. All articles were evaluated using the JBI critical\nappraisal checklist for cohort studies. All four articles were found to have a minimal risk of bias, with scores\nabove 70%. No articles were excluded based on the JBI checklists.\nFigure \n1\n portrays the selection and screening process.\n \n2023 Westwood et al. Cureus 15(5): e38765. DOI 10.7759/cureus.38765\n2\n of \n8\n\nFIGURE\n 1: PRISMA Flow Diagram of the Selection and Screening\nProcess\nPRISMA: Preferred Reporting Items for Systematic Reviews and Meta-Analyses\nResults\nA total of four articles were retained for this review. All identified articles were retrospective cohort studies\nthat addressed disparities in the surgical management and outcomes of women with endometriosis. The two\nmain concepts that appeared were ethnic and racial inequalities in 1) surgical treatment and 2) surgical\ncomplications. Three articles demonstrated that White women are more likely to have minimally invasive\nsurgeries versus open abdominal surgeries for endometriosis diagnosis or treatment compared to other racial\nand ethnic groups \n[19-22]\n. All four articles found that White patients had lower rates of surgical\ncomplications compared to other racial groups \n[19-22]\n. Each article included different racial and ethnic\ncategories with the most limited racial consideration only evaluating Black and White patients \n[19]\n, while the\nmost inclusive study used American Indian or Alaska Native, Asian, Black or African American, Hispanic,\nNative Hawaiian or Pacific Islander, White, and unknown race to categorize patients \n[22]\n.\nDisparities in Endometriosis Surgical Treatments\n \nHysterectomies can be used in endometriosis treatment and diagnosis, and there are many variations of this\nprocedure, from open abdominal laparoscopy to video-assisted laparoscopic surgery. Although minimally\ninvasive hysterectomies shorten recovery time, decrease the length of hospital admissions, and decrease the\nrisk of complications, there is still a disproportionate use of minimally invasive hysterectomies in White\npatients compared to minority racial and ethnic groups \n[19]\n. An article that specifically evaluated Black and\nWhite patients found that Black patients experienced a significantly higher rate of open hysterectomies\ncompared to White women \n[19]\n. Another study investigating endometriosis treatment used a broader range\nof race and ethnicity categories and found that the highest rates of open hysterectomies occurred in Asian\npatients, followed by Black and Hispanic patients, while White patients again had the lowest rates of open\nabdominal hysterectomies \n[21]\n. A third study found comparable results showing that all racial and ethnic\ngroups, except American Indian or Alaskan Natives, were more likely to have an open abdominal\nhysterectomy instead of a laparoscopic hysterectomy for endometriosis compared to White women \n[22]\n.\nThe study with the broadest race and ethnicity categories explored the outcomes of surgical procedures for\nendometriosis beyond hysterectomies \n[22]\n. They evaluated eight surgical procedures to treat and diagnose\nendometriosis, including hysterectomies, and determined the rates of minimally invasive routes versus\n2023 Westwood et al. Cureus 15(5): e38765. DOI 10.7759/cureus.38765\n3\n of \n8\n\nlaparotomy. When the eight alternative endometriosis surgeries were considered, all racial and ethnic\ngroups, excluding Asians, were more likely than White patients to have an open surgery instead of the\nminimally invasive alternative. When hysterectomies were excluded from the surgical types, Hispanic, Black,\nAsian, and unknown race/ethnicity patients were less likely to receive the minimally invasive surgical\nalternative. Black and Hispanic women had the highest rates of oophorectomy while overall hysterectomy\nrates were highest in White and Native American patients \n[22]\n.\nDisparities in Endometriosis Surgical Complications\nThe disproportionate use of open hysterectomies in non-White patients is accompanied by an increased risk\nof both perioperative and postoperative surgical complications \n[19-22]\n. In the studies evaluating the\nprevalence of major and minor postoperative complications, the Clavien-Dindo classification was used to\ndistinguish major from minor complications \n[19,21]\n. The Clavien-Dindo classification ranks surgical\ncomplication severity based on the therapy type needed to fix the complication. The scale consists of grades\nI, II, IIIa, IIIb, IVa, IVb, and V. Grade 3 and higher are considered major complications and include\ncardiopulmonary arrest, myocardial infarction, venous thromboembolism, cerebrovascular accidents,\npneumonia, renal failure, deep or organ surgical site infection, sepsis, unplanned reoperations, and death.\nGrade 2 and lower were considered minor complications and included blood transfusions, urinary tract\ninfections, and superficial wound infections \n[19,21]\n.\nAfter accounting for confounding variables such as comorbidities and surgical approach, it was found that\nBlack women had a significantly increased likelihood of experiencing major and minor postoperative\ncomplications than their White counterparts \n[19,21]\n. An article specifically evaluating the prevalence of\nlower urinary tract infections post-hysterectomy found that Black patients had higher rates of this\ncomplication than White patients \n[20]\n. This study also found that Black women had more extended hospital\nstays, unplanned readmissions, reoperations, and other adverse events in the 30 days postoperation. A study\nincluding Hispanic, Black, Native Hawaiian or Pacific Islander, and American Indian or Alaska Native women\npatients found that non-White patients were more likely to experience similar complications to those above\npostoperatively than did White patients, with Black patients having the most postoperative complications\n[22]\n.\nIn addition to the increased risk of postoperative complications, Black patients had higher rates of\nperioperative complications compared to other racial groups \n[20,22]\n. Black women experienced higher rates\nof morbidity and mortality during surgery than their White, Hispanic, Native Hawaiian or Pacific Islander,\nAmerican Indian, or Alaska Native counterparts \n[22]\n. Black women also had longer perioperative times than\nWhite women after accounting for confounding variables. Table \n1\n displays the characteristics of the articles\nin the review.\n2023 Westwood et al. Cureus 15(5): e38765. DOI 10.7759/cureus.38765\n4\n of \n8\n\nReference\nStudy\nDesign\nStudy Objective\nRace / Ethnicity\nConsiderations\nMajor Findings \nLimitations\nAlexander,\n2019 \n[19]\nRetrospective\nCohort Study\nEvaluate women getting\nhysterectomies for benign\ngynecologic conditions for\nassociations of race,\nsurgical route of\nhysterectomy, and\npostoperative\ncomplications.\nBlack, White.\nBlack women were most\nlikely to experience major\nand minor complications and\nsurgery via an open\nhysterectomy compared to\nWhite women.\nNot representative\nof all racial groups.\nBretschneider,\n2019 \n[20]\nRetrospective\nCohort Study\nEvaluate postoperative\nhysterectomy patients for\nthe incidence of lower\nurinary tract complications\nand other factors during\nsurgery for benign\ngynecologic indications.\nBlack, Other (Alaska\nNative, American\nIndian, Asian, Native\nHawaiian, Pacific\nIslander), Unknown,\nWhite.\nIncreased risk of urinary tract\ncomplications was\nassociated with Black race,\nendometriosis, and prior\nabdominal surgery after\nhysterectomy for benign\ngynecologic conditions.  \nNot representative\nof all racial groups.\nMultiple groups\ncombined into\n“Other”\nMovilla, 2022\n[21]\nRetrospective\nCohort Study\nEvaluate if complications\nfrom hysterectomy surgery\nfor the treatment of\nendometriosis vary\nbetween different races\nand ethnicities.\nAsian, Black,\nHispanic, White\nWhite patients were most\nlikely to have laparoscopic\nhysterectomies, and Asian\npatients were least likely.\nBlack patients were most\nlikely to have major\ncomplications.  \nPossible sampling\nbias. Excluded\n“unknown/not\nreported” race and\nethnicity women.\nOrlando, 2022\n[22]\nRetrospective\nCohort Study\nInvestigate disparities in\nsurgical interventions or\nsurgical complications for\nendometriosis related\nsurgeries among different\nraces and ethnicities.\nAmerican Indian or\nAlaska Native, Asian,\nBlack or African\nAmerican, Hispanic,\nNative Hawaiian or\nPacific Islander,\nUnknown race, White\nWhite women were most\nlikely to have minimally\ninvasive hysterectomies and\nfewer perioperative\ncomplications than minority\nwomen. \nCould not account\nfor possible\nconfounding\nvariables that were\nnot included in the\ndatabase used to\nobtain patient data.\nTABLE\n 1: Summary of findings of the four selected studies\nDiscussion \nThis scoping review was conducted to evaluate the current literature available that addressed disparities\nassociated with endometriosis diagnosis and treatment. A search of five scientific databases yielded four\narticles that met the inclusion criteria. All four articles showed racial and ethnic disparities in the care of\nwomen with endometriosis.\nTwo common themes across the studies suggested that White women were more likely to receive minimally\ninvasive surgical options than ethnic and racial minorities \n[19,20,22]\n and White women were least likely to\nhave surgical complications from their endometriosis-related surgeries than their racial and ethnic minority\ncounterparts \n[19-22]\n. The disproportionate use of open surgical intervention in minority groups is\nsignificant because the minimally invasive options decrease the morbidity of the surgery compared to the\nopen surgical options \n[23]\n. The lower rates of minimally invasive procedures among minorities likely\npredispose them to more surgical complications and worse outcomes. The expected higher rates of\ncomplications associated with decreased usage of the minimally invasive options were shown in all four\narticles. Minority women are more likely to have minor and major surgical complications, including urinary\ntract infections, urinary tract injuries, pulmonary embolism, and the need for a reoperation \n[19-22]\n.\nPreviously published research supported the existence of racial and ethnic disparities throughout\nhealthcare, despite controlling for socioeconomic factors and disease characterization \n[24]\n. This reinforces\nthe current finding that non-White women receive inadequate endometriosis treatment in comparison to\ntheir White counterparts.\nLimitations \nIncluded Studies\n2023 Westwood et al. Cureus 15(5): e38765. DOI 10.7759/cureus.38765\n5\n of \n8\n\nA limitation of the included studies is that they are all cohort studies that used the American College of\nSurgeons National Surgical Quality Improvement Program (NSQIP) database. The cohort studies depended\non data collection from a database that might have a bias in data collection and other factors that cannot be\ncontrolled, including the location of the facility where the procedure was performed or the experience level\nof the surgeon \n[19]\n. The data evaluated for this study are from the hospitals that report their outcomes to the\nNSQIP. Since all articles used the NSQIP database to obtain their cohort data, the information might not be\nrepresentative of the United States as a whole \n[19-22]\n. Another limitation is that the articles did not address\nthe socioeconomic characteristics of the patients and only addressed surgical diagnosis and treatment of\nendometriosis \n[19-22]\n. Due to this lack of socioeconomic evaluation of the patients, these studies failed to\naddress if the financial status, presence, absence, or type of health insurance held by the patient had an\nimpact on aspects of health outcomes, such as when the patient sought medical evaluation if financial status\nprevented a surgery that was otherwise indicated or the type of surgery selected for each patient. The\navailable studies focused on the surgical aspects of endometriosis, despite the search strategy including all\ndiagnostic and treatment options. The absence of studies that discuss disparities in non-invasive medical\nmanagement and outcomes of endometriosis care highlights the need for further investigation into the\ndisparities in endometrial management.\nReview Process\nThe review process yielded four studies that fit the inclusion criteria, which is a small number when\nconsidering that up to 10% of females have endometriosis, a chronic condition that is associated with\nchronic pain, decreased quality of life, and infertility \n[2]\n. The search was restricted to studies published in\n2015 or later and data collected within the United States, which excluded older studies and some completed\nin other countries. The limitation on publication date excluded other relevant articles. Further, while this\nstudy included a small number of articles, the search strategy through five databases was robust, verified by\nan expert librarian, and conducted based on PRISMA guidelines. The articles were evaluated by multiple\nauthors to determine if they fit the inclusion criteria, and all included articles were evaluated using the JBI\ncritical appraisal tools. The reference list of all four studies was manually searched without revealing any\nadditional relevant articles. \nImplications for practice\nWhile the research studies contained in this review did not determine the cause of the disparity in outcomes\nfor endometriosis treatment, the findings suggest that disparities exist for non-White minority groups. Until\nfurther research and conclusions are made, healthcare professionals and physicians should strive to ensure\nthey provide consistently high-quality and appropriate care to all women seeking endometriosis treatment,\nregardless of race or ethnicity. Each patient should be apprised of all the treatment options and encouraged\nto work with their physician to find the best treatment to limit the risks of complications and adverse\noutcomes.\nFuture research considerations\nThe consensus of the four articles is that racial and ethnic minority females experience more complications\nfrom endometrial-related surgeries and are less likely to receive the laparoscopic surgical option. However,\nthe causes of these findings were not well addressed. Future research should be conducted that aims to\naddress if there are racial or ethnic biases from physicians and healthcare systems toward minority patients.\nFurthermore, studies should evaluate if there are confounding variables, such as socioeconomic or cultural\nfactors, that are affecting the outcomes. Understanding the basis of why disparities exist is necessary to\nimplement changes to correct the imbalance.\nFuture studies should aim to be inclusive of the racial, ethnic, and socioeconomic diversity of females with\nendometriosis. Studies that included only White and Black or White, Black, and Hispanic patients were not\ninclusive of the United States population. Excluding minority groups limits the ability to understand,\naddress, and improve disparities within healthcare. In addition to the inclusivity of race and ethnicity, the\nsocioeconomic factors that affect endometriosis care need further investigation. Exploration of how a lack of\naccess to healthcare and the ability to afford treatment impacts those with endometriosis is necessary to\naddress the disparity and decrease the suffering from this chronic condition.\nThis review only found articles about short-term surgical diagnosis and management related to endometrial\ncare. Since endometriosis is a chronic condition that impacts the quality of life of the affected women,\nfurther evaluation should be conducted to determine if disparities exist in the long-term medical\nmanagement of endometriosis \n[2]\n.\nFinally, to implement lasting strategies to improve and assure sustainable healthcare equity, there needs to\nbe a prioritization of and commitment to conducting extensive, representative, and comprehensive research\non the factors impeding health equity. Among these factors are minority attitudes towards the healthcare\nsystem, barriers faced in accessing quality care, and specific factors influencing provider decisions about the\nroute of care, including provider bias.\n2023 Westwood et al. Cureus 15(5): e38765. DOI 10.7759/cureus.38765\n6\n of \n8\n\nConclusions\nRegarding the diagnosis and surgical management of endometriosis in the United States, the research\nsummarized in this review suggests that Black women face a higher risk of perioperative and postoperative\ncomplications in comparison to White women. Although one study found that American Indian or Alaska\nNative, Asian, Hispanic, and Native Hawaiian or Pacific Islander patients also face an increased risk of\nperioperative and postoperative complications, these racial groups are often overlooked in the current body\nof research. The preventable burden of suboptimal care experienced by non-White women must be further\nexplored, along with contributing systemic and socioeconomic factors (e.g., income, insurance, and access\nto care), to implement best practices to ensure healthcare equity for all patients. Economic, educational,\noccupational, geographic, and sociocultural disparities are both embedded within and partially responsible\nfor the systemic failure to provide minority patients with exceptional care. Non-White women face an\nunnecessary and problematic burden of risk when it comes to receiving quality endometriosis care, despite\ncontrolling for confounding variables.\nAdditional Information\nDisclosures\nConflicts of interest:\n In compliance with the ICMJE uniform disclosure form, all authors declare the\nfollowing: \nPayment/services info:\n All authors have declared that no financial support was received from\nany organization for the submitted work. \nFinancial relationships:\n All authors have declared that they have\nno financial relationships at present or within the previous three years with any organizations that might\nhave an interest in the submitted work. \nOther relationships:\n All authors have declared that there are no\nother relationships or activities that could appear to have influenced the submitted work.\nReferences\n1\n. \nShafrir AL, Farland LV, Shah DK, Harris HR, Kvaskoff M, Zondervan K, Missmer SA: \nRisk for and\nconsequences of endometriosis: a critical epidemiologic review\n. 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