Racial Disparities in Minimally Invasive Benign Hysterectomy.

Background and Objectives: Racial and ethnic disparities in access to minimally invasive surgery (MIS) and the rate of surgical complications in minority groups remain profoundly underinvestigated. This meta-analysis aims to compare the rate of MIS utilization for benign hysterectomy as well as the surgical morbidity among racial and ethnic minority patients in the United States.

Studies comparing utilization rate of MIS for benign hysterectomy among non-Hispanic white, Black, and Hispanic populations were considered eligible. The primary outcome was the rate of MIS according to race. The secondary outcome was surgical morbidity risk (Clavien-Dindo Classification) according to hysterectomy route and race. Random-effect model meta-analysis pooled unadjusted and adjusted odds ratios (ORs) with 95% confidence intervals (CIs).

Thirteen studies were eligible, with a total of 1,123,851 patients undergoing benign hysterectomy, of whom 817,209 were white, 187,488 Black, and 119,154 Hispanic. Black and Hispanic patients were less likely to undergo MIS compared to white patients (Black: OR 0.44 [95% CI 0.39–0.49] and Hispanic: OR 0.65 [95% CI 0.59–0.71]). After pooling adjusted estimates, the rate of MIS use remained significantly lower in nonwhite populations. Nonwhite patients were more likely to develop surgical complications after hysterectomy in either MIS (OR 1.32 [95% CI: 1.15–1.52]) or open hysterectomy (OR 1.56 [95% CI: 1.40–1.73]).

Racial and ethnic disparities in MIS utilization for benign hysterectomy are strikingly apparent in the United States, with nonwhite patients often demonstrating lower access to MIS utilization and higher rates of surgical morbidity than white patients.

Disparity, Ethnicity, Hysterectomy, Minimally invasive, Race

Hysterectomy remains the most common gynecologic surgery in the United States (US).1 While open hysterectomy used to be the most practiced approach,2,3 minimally invasive surgery (MIS), including vaginal, laparoscopic, and robotic-assisted approaches to hysterectomy, gained substantial popularity given the overwhelming evidence of its advantages, including shorter recovery time and fewer perioperative complications.4 Despite previous efforts demonstrating racial disparities in the utilization of MIS for hysterectomy,1,5–7 discrepancies were observed. For example, Schneyer et al6 showed MIS utilization rates of 59.8% and 44.0% in white and Black women, respectively, whereas Su et al showed rates of 80.4% and 65.3% for the same respective groups that were nonstatistically significant after adjusting for patient-level factors such as uterine weight.7 Of note, racial disparities have also been observed in the complication rate of benign hysterectomy,1,5,6 but it remains unclear whether these disparities are an extension of disparities in MIS utilization rate, differences in the complexity of underlying pathology, or a combination of both. Therefore, and in order to provide consistent evidence and enhanced understanding of the true racial and ethnic disparities in minimally invasive hysterectomy, there is a need to compile the existing evidence regarding MIS utilization rate among different racial and ethnic groups. This systematic review and meta-analysis aims to: (1) compare the overall rate of MIS utilization and (2) compare the overall surgical morbidity after benign hysterectomy based on patients’ race and ethnicity in the US.

This systematic review and meta-analysis were conducted according to the Preferred Reporting Items for Systematic Reviews and Meta-Analyses (PRISMA) checklist.8 The study protocol for this systematic review was registered in the PROSPERO international prospective register of systematic reviews. Information Sources and Search Strategy A literature search was conducted by 2 independent authors (K.H. and M.A.B.) in the following databases: Medline, EMBASE, and Web of Science from their inception to September 20th, 2022. The reference lists of retrieved articles were also evaluated. The following search terms were used: (“racial” OR “minority” OR “race” OR “ethnicity” OR “black*” OR “white” OR “African American” OR “Caucasian” OR “Hispanic” OR “Latin*” OR “Asian” OR “native*” OR “pacific*”) AND (“minimally invasive gynecol*” OR “laparoscopic hyster*” OR (“laparoscop*” AND “Gynecol”). No restrictions for language were applied. Inclusion and Exclusion Criteria Studies examining racial and ethnic disparities in MIS utilization for hysterectomy were considered eligible if they met the following criteria: (1) the study had a prospective or retrospective cohort, case-control, or cross-sectional design, (2) included patients undergoing hysterectomy for benign indications in the US, and (3) investigated associations between race/ethnicity and surgical route, as well as surgical morbidity—considering nonwhite race as the risk factor and white race as the comparator. Studies of patients undergoing hysterectomy for gynecologic cancer, patients undergoing surgery outside of the US, or patients selected from randomized controlled trials or case-reports or case-series were excluded. Selected studies were reviewed for eligibility by 2 independent authors (K.H. and M.A.B.); discrepancies between reviewers were resolved by consensus or by consulting a third investigator. According to the PICO criteria, Population was women undergoing hysterectomy for benign conditions, Intervention was hysterectomy, Comparison was performed according to patients’ race and ethnicity, and Outcome was the utilization rate of MIS for hysterectomy. Outcome Measure The primary outcome was the rate of MIS for benign hysterectomy among various racial and ethnic groups. The secondary outcome was surgical morbidity associated with benign hysterectomy according to race or ethnicity and surgical route (MIS vs open). The Clavien-Dindo grading scale was used to identify surgical morbidity.9 Major complications included venous thromboembolism, myocardial infarction, stroke, pneumonia, deep or organ surgical site infection, fascial dehiscence, and any complication, such as organ injury requiring reoperation, acute renal failure, sepsis, cardiopulmonary arrest, intubation greater than 48 hours, death from the operation, and/or readmission. Minor complications included urinary tract infection, superficial wound infection, and/or blood transfusions. Patients were considered to have any surgical morbidity if they had at least one major or minor complication. Quality Assessment The quality of each included study was assessed by reviewers according to the Newcastle-Ottawa Scale (NOS) criteria for observational studies. The NOS contains 3 sections: selection, comparability, and outcome or exposure—designed to gauge the risk of bias in nonrandomized studies. A score above 7 confers high quality.10 Statistical Analysis Random-effects model was used to compare the rates of MIS utilization for hysterectomy and surgical morbidity among different racial and ethnic populations (Black and Hispanic vs white population) using unadjusted and adjusted estimates. Adjustments for confounding variables in each study are outlined in Table 1. Additionally, Black and Hispanic patients were assigned to an umbrella group of nonwhite patients and compared to the white group in terms of MIS utilization for hysterectomy and risk of surgical morbidity. We used the I2 statistic to assess heterogeneity. In order to assess the influence of individual studies on the pooled result as well as heterogeneity, we conducted a sensitivity analysis by excluding each study sequentially and recalculating the combined estimates on the remaining studies. We used STATA v.17 (StataCorp LLC, College Station, Texas) for data analysis and graph generation. Table 1. | Study | Study Design | Time Frame | Location | Database | Sample Size White | Sample Size Black | Sample Size Hispanic | Indication of Hysterectomy | Adjustment | NOS Quality Assessment | |---|---|---|---|---|---|---|---|---|---|---| | Schneyer et al (2022) | Retrospective cohort | 2015–2020 | Los Angeles | Cedars-Sinai Medical Center | 525 | 366 | 184 | Leiomyoma | Age, body mass index, American Society of Anesthesiology class, parity, prior laparotomies, preoperative anemia, insurance type, and uterine size | 7 | | Su et al (2022) | Prospective cohort | 2015–2017 | Detroit | Henry Ford Health System | 235 | 196 | N/A | Any | Uterine weight and surgery reason is fibroids | 7 | | Ko et al (2020) | Retrospective cohort | 2014–2017 | US-nationwide | American College of SurgeonsNational Surgical Quality Improvement Program (NSQIP) | 8,326 | 6,474 | 2,162 | Leiomyoma | Age, body mass index, diabetes, smoking history, hypertension, Charlson comorbidity index, parity, uterine weight >250 g or not, endometriosis, pelvic inflammatory disease, previous abdominal operation, previous pelvic operation, elective surgery or not, and additional procedures at time of hysterectomy | 9 | | Alexander et al (2019) | Retrospective cohort | 2015 | US-nationwide | American College of Surgeons National Surgical Quality Improvement Program (NSQIP) | 11,330 | 3,806 | N/A | Any benign indication | Prior abdominal surgery, pelvic surgery, endometriosis, BMI, age, and comorbidity | 8 | | Pollack et al (2019) | Cross-sectional | 2010–2014 | US-nationwide | Healthcare Research and Quality Healthcare Cost and Utilization Project (HCUP) | 98,700 | 8,810 | 15,965 | Any | N/A* | 6 | | Lonky et al (2017) | Retrospective cohort | 2010–2011 | California | Kaiser Permanente Southern California (KPSC) dataset | 1,065 | 579 | 1,186 | Any | N/A* | 7 | | Price et al (2017) | Cross-sectional | 2010–2013 | Philadelphia | Academic hospitals within the University of Pennsylvania Health System in Philadelphia | 659 | 978 | N/A | Fibroids and/or abnormal uterine bleeding | Age, body mass index, procedure year, hospital, obstetrical and surgical history, primary diagnosis, uterine weight, and all other variables reported (race, ethnicity, median household income quartile, insurance status) | 7 | | Sanei-Moghaddam et al (2017) | Retrospective cohort | 2012–2014 | Pennsylvania | UPMC-affiliated hospitals | 5,653 | 702 | N/A | Any | N/A* | 6 | | Mehta et al (2017) | NR | 2012–2014 | Maryland | The Maryland Health Services Cost Review Commission (HSCRC) database. | 2,405 | 2,473 | 102 | Any | Surgeon hysterectomy volume, hospital hysterectomy volume, hospital bed size, surgeon practicing year, patient age, patient race, payer, Elixhauser score, and benign indications | 8 | | Cohen et al (2014) | Cross-sectional | 2009 | US-Nationwide | NIS | 237,870 | 57,810 | 39,501 | FibroidsEndometriosisProlapse | Age, indication surgery, urban–rural location, household income, hospital bed size, insurance, region of hospital, and comorbidity | 8 | | Patel et al (2013) | Retrospective cohort | 2010 | US-Nationwide | NIS | 15,571 | 7,495 | 3,671 | Menorrhagia or leiomyoma | N/A* | 7 | | Jacoby et al (2009) | Cross-sectional | 2005 | US-Nationwide | NIS | 267,465 | 49,195 | 37,164 | FibroidsEndometriosisPelvic infectionProlapseAbnormal bleeding | Age, income, region, hospital setting, indication surgery, insurance, and hospital bed size | 9 | | Abenhaim et al (2008) | Retrospective cohort | 1998–2002 | US-Nationwide | NIS | 167,405 | 48,604 | 19,219 | Uterine leiomyomas or menorrhagia | Age, type of hospital, admission type, and comorbid illnesses | 8 | Notes. *No adjustment specifically for MIS utilization rate.

Literature Search A total of 1,445 articles were retrieved (Figure 1). Of these, 244 articles were excluded for duplication and the remaining 1,197 studies were screened for eligibility. Title and abstract screening resulted in 39 potentially eligible studies. After a full-text assessment was conducted, 13 studies met the inclusion criteria defined above. Characteristics of Included Studies The characteristics of included studies are summarized in Table 1. Included studies were published between 2008 and 2022. Seven studies were retrospective studies,1,6,11–15 four were cross-sectional studies,5,16–18 one was a prospective cohort study,7 and one study had no reported design.19 Seven studies presented national-level data,1,5,11,13,15,16,18 whereas six studies were conducted in state-level populations.6,7,12,14,17,19 The risk of bias was low in most studies; six studies had a low risk of bias, five had a moderate risk of bias with NOS score of 7, and two studies had score of 6 (Table 1). Racial and Ethnic Disparity in MIS Utilization for Benign Hysterectomy Compared to white patients, rates of MIS utilization for hysterectomy were significantly lower among nonwhite patients (odds ratio [OR] 0.50, 95% confidence interval [CI]: 0.45–0.56, P < 0.001, I2 = 98.6%), including Black (OR 0.44, 95% CI: 0.39–0.49, P < 0.001, I2 = 98.2%) and Hispanic (OR 0.65, 95% CI: 0.59–0.71, P < 0.001, I2 = 96.8%) patients (Figure 2). After pooling adjusted estimates, the rate of MIS utilization for hysterectomy remained significantly lower among Black (OR 0.56 [95% CI: 0.43–0.72], P < 0.001, I2 = 95.8%) and Hispanic (OR 0.58 [95% CI: 0.51–0.67], P < 0.001, I2 = 66.8%) patients (Figure 3). The overall heterogeneity and effect sizes did not significantly change after sensitivity analyses through one-by-one exclusion. Racial and Ethnic Disparity in Surgical Morbidity after Benign Hysterectomy Black and Hispanic patients were more likely to experience surgical morbidity after benign hysterectomy compared to white patients (OR 1.79, 95% CI: 1.66–1.93, P < 0.001, I2 = 0.0%; OR 1.43, 95% CI: 1.08–1.89, P = 0.013, I2 = 46.0%, respectively) (Figures 4B and 4C). Black patients were at an increased risk of surgical morbidity regardless of surgical route, including open (OR 1.61, 95% CI: 1.45–1.80, P < 0.001, I2 = 0.0%) and MIS (OR 1.35, 95% CI: 1.11–1.65, P = 0.003, I2 = 61.7%) (Figures 5B and 6B). Only one study examined the risk of surgical morbidity by hysterectomy route among Hispanic patients, which showed a comparable morbidity risk to white patients (Figures 5C and 6C).

Brief Summary of Results This systematic review found that the rate of MIS utilization for benign hysterectomy in the US significantly varies among racial groups. White patients are more likely to undergo minimally invasive hysterectomy than nonwhite patients, including Black and Hispanic patients. This remains true despite adjusting for age, body mass index, prior abdominal surgery, uterine weight, and indication for surgery. Additionally, Black patients have a 1.7-fold increase in risk of experiencing surgical morbidity defined as one minor or one major complication, regardless of the surgical route of hysterectomy. Hispanic patients also demonstrated a greater morbidity after benign hysterectomy. Relevance and Context of What is Known This study is the first meta-analysis exploring the racial disparity in MIS utilization for benign hysterectomy. While the overall rate of minimally invasive hysterectomy remains low at less than 50%, this rate is even lower among nonwhite patients and persists despite pooling adjusted estimates. Prior reports have attributed lower rates of minimally invasive hysterectomy approaches among Black women to their higher risk of having fibroids and larger uterine volumes.21 Notably, however, these disparities persisted despite adjusting for these factors, emphasizing an inherent socioeconomic basis to these disparities.22 Geographic factors contributing to these disparities include the lack of MIS-equipped hospitals and MIS-trained surgeons in rural counties, where certain racial and ethnic minorities are more likely to reside, as well as the large geographic distance from large hospitals, where these advanced facilities and surgeons exist.23,24 Strengths and Limitations Strengths of this systematic review include its extensive review of the comparative literature by 2 independent authors. With 13 studies included in this meta-analysis, the sample size was large and the outcomes of each study was homogenous. Thus, this study was able to emphasize the racial disparity in the use of MIS for benign hysterectomy. Additionally, given overall low complication rate in minimally invasive hysterectomy and limited studies reporting them among different racial groups, this meta-analysis provides valuable pooled data to better understand the distribution and risk of surgical complications after minimally invasive hysterectomy among ethnic and racial minority groups. On the other hand, this review was not able to fully capture the prevalence of hysterectomy among Asian or Native American women given the small number of studies reporting data on Asian women or “other” race categories. Outcome on Clinical Practice/Future Studies With the increasing rate of a MIS approaches to benign hysterectomy, minimally invasive gynecologic surgeons, and the well-recognized faster recovery of and low surgical morbidity with MIS, it is substantial to offer minimally invasive approaches whenever feasible across all patient groups and delineate access barriers to minimally invasive hysterectomy.20 The driver of the current disparities in utilizing minimally invasive hysterectomy is largely unknown and warrants further exploration to eliminate these disparities and align with the Obstetrics and Gynecology Joint statement.21 In their study, Smith et al have proposed several valuable approaches to minimizing disparities in utilizing robotic hysterectomy.22 For example, utilizing standardized algorithms in surgical decision making and candidate selection for minimally invasive hysterectomy could help eliminate implicit biases contributing to unjust allocation of hysterectomy approaches among certain racial and ethnic groups.25 In addition, incorporating surgical mentorships, especially in smaller, rural hospitals, has proved effective in increasing rates of minimally invasive hysterectomy.26 This was derived from the observation that the rates of robotic hysterectomy were highest among women operated on in large, teaching hospitals irrespective of race.22 Further, while direct patient marketing and interhospital regional competition have enhanced uptake of minimally invasive hysterectomy, it is paramount to ensure equal awareness of all racial and ethnic groups, and not only privileged populations, of the availability of these options, which otherwise would be counterproductive to eliminating access disparities.27,28 Of note, given the wider adoption of these minimally invasive approaches to hysterectomy over the recent years, it is crucial to reproduce the disparity data in a more recent timeframe to better understand potential variations in disparity trends in larger populations and wider geographic sections.

Racial and ethnic disparities in MIS utilization for benign hysterectomy are apparent, with lower rates of MIS and higher rates of surgical morbidity in nonwhite patients compared to white patients. Further investigation into the drivers and possible mitigators of these disparities is strongly warranted to allow for fair distribution of gynecologic advancements among all rachial and ethnic patient groups. Footnotes Disclosure: none. Funding sources: none. Conflict of interests: none. Systematic review registration number: CRD42022377382. Contributor Information Kamran Hessami, Department of Obstetrics and Gynecology, Baylor College of Medicine, Houston, Texas. (Dr. Hessami). Marie-Claire Leaf, Department of Gynecology and Obstetrics, Johns Hopkins University, Baltimore, Maryland. (Drs. Leaf, Liang, and Borahay). Jinxiao Liang, Department of Gynecology and Obstetrics, Johns Hopkins University, Baltimore, Maryland. (Drs. Leaf, Liang, and Borahay). Adi Katz, Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra Northwell, Lenox Hill Hospital, New York, New York. (Drs. Katz and Chervenak). Frank Chervenak, Department of Obstetrics and Gynecology, Donald and Barbara Zucker School of Medicine at Hofstra Northwell, Lenox Hill Hospital, New York, New York. (Drs. Katz and Chervenak). Abdelrahman AlAshqar, Department of Obstetrics, Gynecology and Reproductive Sciences, Yale School of Medicine, New Haven, Connecticut. (Dr. AlAshqar). Mostafa A. Borahay, Department of Gynecology and Obstetrics, Johns Hopkins University, Baltimore, Maryland. (Drs. Leaf, Liang, and Borahay).

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