Abstract
Objective:
To estimate the associations between race, route of hysterectomy and postoperative complications among women undergoing benign hysterectomy.
Methods:
A cohort study was performed. All patients undergoing benign hysterectomy, recorded in the National Surgical Quality Improvement Program (NSQIP) and its targeted hysterectomy file in 2015, were identified. The primary exposure was patient race. The primary outcome was route of hysterectomy and the secondary outcome was postoperative complication. Associations were examined using both bivariable tests and logistic regression.
Results:
Of 15,136 women who underwent benign hysterectomy, 75% were white and 25% were black. Black women were more likely to undergo an open hysterectomy than white women (50.1% vs. 22.9%; OR: 3.36, 95%CI: 3.11–3.64). Black women had larger uteri (median 262g vs. 123g; 60.7% vs. 25.6% with uterus >250g), more prior pelvic surgery (58.5% vs. 53.2%) and higher BMIs (32.7 vs. 30.4). After adjusting for these and other clinical factors, black women remained more likely to undergo an open hysterectomy (aOR: 2.02, 95%CI: 1.85–2.20). Black women experienced more major complications than white women (4.1% vs. 2.3%; p<0.001) and more minor complications (11.4% vs. 6.7%; OR: 1.78, p<0.001). Again these disparities persisted with adjustment (major aOR: 1.56, 95%CI: 1.25–1.95; minor aOR: 1.27, 95%CI: 1.11–1.47).
Conclusions:
Back women have a higher proportion of open hysterectomy and experience more major and minor postoperative complications. These differences persisted even after adjusting for confounding medical, surgical, and gynecologic factors.
Precis:
Black women undergoing benign hysterectomy undergo a higher proportion of open surgery and have more surgical complications when compared to white women.
Introduction:
Hysterectomy is the second most common surgical procedure performed on women in the United States.1 Since the early 2000s there has been a trend towards performing hysterectomy using a minimally invasive approach – either laparoscopic or vaginal, as studies have shown lower costs, fewer complications, and faster recovery times.2 Racial disparities persist in the US particularly with regard to implementation of new medical care or novel surgical technology.3 Several studies have shown that black race, in particular, is associated with decreased odds of receiving minimally invasive hysterectomy in patients with both benign or cancerous conditions.4,5
Several recent papers suggesting disparities in the route of hysterectomy have utilized secondary datasets that do not account for differences in patient populations.6–8 In particular, black women have two to three times risk of developing uterine fibroids and, as a result, may have larger uteri, which could contribute to higher rates of open hysterectomies.9 Additionally, black women have higher rates of co-morbidities, such as obesity, diabetes, and hypertension, which may also contribute to higher rates of open hysterectomy.10,11 However, it is unclear if disparities in route of hysterectomy persist for black women after accounting for patient factors, such as BMI, uterine size and prior pelvic surgery, all factors which may predispose a surgeon to perform an open hysterectomy, as these variables are not available previously used datasets.
The objectives of this study are to determine the associations between race and route of hysterectomy and between race and postoperative complications, among women undergoing benign hysterectomy.
Methods
A cohort study was performed using prospectively collected data. Patients who underwent hysterectomy for any benign condition during 2015 were identified using International Classification of Diseases, 9th revision codes and Current Procedural Terminology (CPT) codes from the hysterectomy specific file of the American College of Surgeons National Surgical Quality Improvement Program (NSQIP) Database. The institutional review board at Northwestern University reviewed this study and deemed it exempt from formal review as all data previously existed and was also deidentified
Participation in NSQIP is voluntary and data are used by each participating hospital to track and measure surgical outcomes. Patient-level data such as demographics, perioperative measures and post-operative outcomes are collected from electronic health records by specially trained clinical nurse reviewers. The data are periodically audited to maintain accuracy, however, it is important to note that data quality is excellent with participating institutions having only 2% intra-observer disagreement.12 Details of methods of data collection and reliability have been previously published.13
The primary outcome was route of hysterectomy, either minimally invasive (total laparoscopic, laparoscopically assisted vaginal, robotic, or vaginal hysterectomy) or open abdominal (total abdominal hysterectomy). The key exposure was patient race, either black or white. Surgical complications are secondary outcomes, which were defined as complications occurring from surgery up to 30 days following postoperatively. Similar to previously published studies, complications were classified as major or minor, using the validated Clavien-Dindo grading scale; major complications were defined as grade 3 or higher, minor complications were defined as grade 2 or lower.14,15 Major complications included venous thromboembolism, myocardial infarction, stroke, pneumonia, deep or organ surgical-site infection, fascial dehiscence, unplanned return to the operating room, renal failure, sepsis, cardio-pulmonary arrest, intubation greater than 48 hours and death. Minor complications included urinary tract infection, superficial wound infection and blood transfusion. The diagnostic criteria used to define each of these complications is published in the NSQIP data participant use file.16
Black patients were compared to white patients with respect to outcomes (hysterectomy route and complications). For bivariate comparisons, 2-tailed t-tests were used for continuous variables, Kruskal Wallis for non-parametric variables, and Pearson Χ2 test for categorical variables. Association between race and route of hysterectomy were analyzed using binary logistic regression for potential confounding. Confounders were defined a priori and were selected by considering clinical factors that may be taken into consideration when selecting route of hysterectomy including uterine weight, prior abdominal or pelvic surgery, endometriosis, BMI, age, and comorbidities.17–19 Although uterine weight can only be assessed after hysterectomy, it is the best measurement of uterine size. We tested uterine weight as a continuous, categorical (<250g, 250–499g, 500–100g and >1000g) and binary (<250g, ≥250g) variable. Modeling uterine weight in different ways resulted in little variation to the adjusted odds ratio and overall model fit. Ultimately, we chose to model uterine weight as a binary variable, either smaller or greater than 250 grams, as most clinicians are able to approximate uterine size as large or small, based on clinical exam prior to surgery and because 250 grams has been used as a benchmark for higher reimbursement, due to greater surgical complexity.20
In examining the association of black race and postoperative complications, a stratified analysis by route of hysterectomy was performed, as our first analysis showed an association between route of hysterectomy and both race and postoperative complications. For this model, confounders were again defined a priori by selecting clinical factors that are known to be associated with postoperative complications. The factors accounted for included: prior abdominal surgery, prior pelvic surgery, endometriosis, BMI, age, comorbidities, procedures performed at the time of hysterectomy and route of hysterectomy (open versus minimally invasive).14,15
Sensitivity analyses were performed to ensure our models were robust and sensitive to variations in how the uterine weight variable was categorized. First, given the large difference in median uterine weight of black versus white women, we limited our analysis to women with uterine weight less than 250g for both races to examine the possibility that uterine weight drives our adjusted analysis. Second, despite our large dataset we recognized that complications are rare events, in particular major complications. Therefore, propensity score matching was undertaken to create a cohort where black and white subjects were balanced on the same factors accounted for in our logistic regression: prior abdominal surgery, prior pelvic surgery, endometriosis, BMI, age, comorbidities, procedures performed at the time of hysterectomy and, in our final analysis, route of hysterectomy (open versus minimally invasive). A p value of less than 0.05 was considered significant for all analysis. STATA version 14.1 (StataCorp, College Station, TX) was used for all analysis.
Results
A total of 15,316 patients were identified in the hysterectomy specific file of the NSQIP Database. Patient demographic characteristics and past medical, surgical, and gynecologic history are shown in Table 1. The study population consisted of 74.9% (n= 11,330) white and 25.1% (n=3806) black patients. Black patients were younger, had a higher BMI, were more likely to have diabetes and hypertension, had a higher median uterine weight, and a higher incidence of prior abdominal surgery. However, white patients were more likely to have a diagnosis of endometriosis and have a history of prior pelvic surgery.
Table 1:
Patient Characteristics
| Overall n= 15,136 |
White Race n= 11,330 |
Black Race n=3806 |
P value | |
|---|---|---|---|---|
| Open Hysterectomy | 4,502 (29.7) | 2,597 (22.9) | 1905 (50.1) | <0.001 |
| MIS Hysterectomy | 10,634 (70.3) | 8,733 (77.1) | 1901 (49.9) | <0.001 |
| Vaginal | 2,374 (15.7) | 2,019 (17.8) | 355 (9.4) | <0.001 |
| Laparoscopic | 8,259 (54.6) | 6,714 (59.3) | 1,545 (40.5) | <0.001 |
| Age, y | 47.1 +/− 11.0 | 48.1 +/− 11.5 | 44.1 +/−8.7 | <0.001 |
| 18–29 | 431 (2.9) | 314 (2.8) | 117 (3.1) | 0.33 |
| 30–39 | 3,189 (21.1) | 2,187 (19.3) | 1,002 (26.3) | <0.001 |
| 40–49 | 6,412 (42.4) | 4,497 (39.7) | 1,1915 (50.3) | <0.001 |
| 50–59 | 2,974 (19.7) | 2,414 (21.3) | 560 (14.7) | <0.001 |
| 60–69 | 1,448 (9.6) | 1,286 (11.35) | 162 (4.3) | <0.001 |
| 70+ | 682 (4.5) | 632 (5.6) | 50 (1.3) | <0.001 |
| BMI, kg/m2 | 30.9 +/− 7.7 | 30.4 +/− 7.7 | 32.7 +/− 7.6 | <0.001 |
| Underweight (>18) | 104 (0.7) | 82 (0.7) | 22 (0.6) | 0.35 |
| Normal (18–25) | 3,399 (22.5) | 2,894 (25.5) | 505 (13.3) | <0.001 |
| Overweight (25–30) | 4,394 (29.0) | 3,356 (29.6) | 1,038 (27.3) | 0.01 |
| Obesity I (30–35) | 3,381 (22.3) | 2,389 (21.1) | 992 (26.1) | <0.0001 |
| Obesity II (35–40) | 1,973 (13.0) | 1,331 (11.8) | 642 (16.9) | <0.0001 |
| Obesity III (40–50) | 1,481 (9.8) | 996 (8.8) | 485 (12.7) | <0.0001 |
| Extreme Obesity (50+) | 404 (2.7) | 122 (3.2) | 282 (2.5) | 0.02 |
| Smoker* | 2,448 (16.2) | 1806 (15.9) | 642 (16.9) | 0.17 |
| Diabetes | 1,150 (7.6) | 820 (7.2) | 330 (8.7) | 0.01 |
| Hypertension | 4,098 (27.7) | 2,749 (24.3) | 1,349 (35.4) | <0.001 |
| Charlson Comorbidity Index Score | ||||
| 0 | 13,812 (91.3) | 10,369 (91.5) | 3,443 (90.5) | 0.05 |
| 1 | 1,214 (8.0) | 880 (7.7) | 334 (8.8) | 0.05 |
| ≥2 | 110 (0.7) | 81 (0.71) | 29 (0.8) | 0.77 |
| Gynecologic History | ||||
| Parity | 2(1–3) | 2 (1–3) | 2 (0–3) | <0.001 |
| Uterine Weight (g) | 140 +/− 92 | 123 +/−115 | 262 +/−203 | <0.001 |
| Uterine Weight >250g | 5,210 (38.4) | 2,899 (25.6) | 2,311 (60.7) | <0.001 |
| Endometriosis | 1,806 (11.9) | 1,435 (12.7) | 371 (9.8) | <0.001 |
| Pelvic Inflammatory Disease | 249 (1.6) | 172 (1.5) | 77 (2.0) | 0.03 |
| Surgical History | ||||
| Prior Abdominal Surgery | 3,992 (26.4) | 3,256 (28.7) | 736 (19.3) | <0.001 |
| Prior Pelvic Surgery | 8,249 (54.5) | 6,022 (53.2) | 2,227 (58.5) | <0.001 |
Smoking defined as current smoker or smoker within the last year.
Data presented as n(%) for categorical variables, mean +/− SD for continuous variables, median and range for skewed variables
Overall, more patients underwent minimally invasive hysterectomy (n=10,634, 70.3%) than open hysterectomy (n=4,502, 29.7%). Black women underwent a higher proportion of open hysterectomy (50.1%), compared to white women (22.0%) (OR: 3.36, 95% CI: 3.11–3.64).
After using a logistic regression to adjust for the factors associated with the selection of open hysterectomy, regardless of race, black women still had twice the odds of having an open hysterectomy compared to white women (Table 2). When the analysis was limited to only women with small uterine size (weight <250g), black women remained at significantly higher odds of undergoing open hysterectomy (aOR 1.84, 95%CI 1.61–2.11, Table 3).
Table 2:
Association between Race and Open Surgery
| N (%) | Unadjusted OR | 95% CI | Adjusted OR* | 95%CI | |
|---|---|---|---|---|---|
| White Race | n= 11,330 | 1 (ref) | 1 (ref) | ||
| Black Race | n=3806 | 3.36 | 3.11–3.64 | 2.02 | 1.85–2.20 |
Multivariable logistic regression model adjusted for uterine weight, prior abdominal surgery, pelvic surgery, endometriosis, BMI, age and comorbidity
Table 3:
Association between Race and Open Surgery, Limited to Patients with Uterine Weight <250g
| N (%) | Unadjusted OR | 95% CI | Adjusted OR* | 95%CI | |
|---|---|---|---|---|---|
| White Race | n= 8.431 | 1 (ref) | 1 (ref) | ||
| Black Race | n=1,495 | 1.92 | 3.11–3.64 | 1.84 | 1.61–2.11 |
Multivariable logistic regression model adjusted for prior abdominal surgery, pelvic surgery, endometriosis, BMI, age and comorbidity
A larger proportion of black women experienced complications when undergoing hysterectomy compared to white women, though stratified analysis showed that the proportion varied by type of hysterectomy (Table 4). When considering all modes of hysterectomy black women experienced more total complications (14.1% vs. 8.6%, p<0.001), more major complications (4.1 vs. 2.4%, p<0.001) and more minor complications (11.4% vs. 6.7%, p<0.001). When examining patients who underwent vaginal hysterectomy there were no differences in the proportion of women who had complications for black versus white women, though there was a small number of complications. When examining only open hysterectomy, black women had greater number of minor complications (16.9% vs 11.3%, p<0.001). Lastly, when women underwent laparoscopic hysterectomy, black women had more major complications when compared to white women (3.3% vs 1.8%, p<0.001).
Table 4:
Bivariate Comparison of Complications by Race Stratified by Method of Hysterectomy
| Total Complications n (%) |
p-value | Minor Complications n (%) |
p-value | Major Complications n (%) |
p-value | |
|---|---|---|---|---|---|---|
| All Hysterectomies | ||||||
| Black Race | 537 (14.1) | <0.001 | 433 (11.4) | <0.001 | 153 (4.1 | <0.001 |
| White Race | 973 (8.6) | 760 (6.7) | 265 (2.3) | |||
| Open | ||||||
| Black Race | 376 (19.4) | <0.001 | 322 (16.9) | <0.001 | 94 (4.9) | 0.06 |
| White Race | 357 (13.8) | 289 (11.1) | 98 (3.8) | |||
| Vaginal | ||||||
| Black Race | 36 (10.14) | 0.82 | 28 (7.9) | 0.97 | 9 (2.5) | 0.81 |
| White Race | 197 (9.76) | 158 (7.8) | 47 (2.3) | |||
| Laparoscopic | ||||||
| Black Race | 125 (8.09) | 0.01 | 83 (5.4) | 0.24 | 50 (3.32) | <0.001 |
| White Race | 419 (6.24) | 313 (4.7) | 120 (1.79) | |||
| All Minimally Invasive Hysterectomy | ||||||
| Black Race | 161 (8.5) | 0.03 | 111 (5.8) | 0.44 | 59 (3.1) | <0.001 |
| White Race | 616 (7.1) | 471 (5.4) | 167 (1.9) | |||
To adjust for factors that might place a patient at higher odds of developing a complication, a logistic regression was performed (Table 5). The regression showed that after adjustment for clinical factors black women still had higher odds of postoperative complications, though the odds were decreased (major aOR: 1.56, CI: 1.25–1.95, minor aOR: 1.27, CI: 1.11–1.47).
Table 5:
The Odds of Having a Complication Given Black Race, Stratified by Route of Surgery
| Unadjusted OR | 95% CI | Adjusted OR* | 95%CI | Propensity Matched Cohort OR | 95% CI | |
|---|---|---|---|---|---|---|
| MIS Hysterectomy | ||||||
| Minor Complication | 1.09 | 0.88–1.35 | 1.06 | 0.85–1.32 | 0.99 | 0.75–1.31 |
| Major Complication | 1.64 | 1.22–2.22 | 1.70 | 1.24–2.34 | 1.27 | 0.86–1.88 |
| All Complications | 1.21 | 1.02–1.46 | 1.20 | 1.01–1.48 | 1.10 | 0.87–1.39 |
| Open Hysterectomy | ||||||
| Minor Complication | 1.62 | 1.37–1.93 | 1.43 | 1.19–1.73 | 1.35 | 1.10–1.66 |
| Major Complication | 1.48 | 0.99–1.77 | 1.48 | 1.08–2.04 | 1.47 | 1.01–2.15 |
| All complications | 1.54 | 1.32–1.81 | 1.46 | 1.23–1.75 | 1.41 | 1.16–1.71 |
| All Hysterectomy | ||||||
| Minor Complication | 1.78 | 1.57–2.02 | 1.27** | 1.11–1.47 | 1.22** | 1.03–1.44 |
| Major Complication | 1.75 | 1.42–2.14 | 1.56** | 1.25–1.95 | 1.22** | 0.94–1.58 |
| All Complications | 1.75 | 1.56–1.96 | 1.35** | 1.17–1.51 | 1.25** | 1.08–1.46 |
Adjusted for uterine weight, prior abdominal surgery, pelvic surgery, endometriosis, BMI, age, comorbidity and additional procedures at time of hysterectomy
Also adjusted for route of surgery
In the propensity score matched cohort analysis there were no significant differences in patient characteristics that persisted after nearest neighbor matching (all p values >0.05) between the matched cohort of black and white women (Table 6). Regression performed within this cohort largely confirmed the findings from the multivariable logistic regression: black women remained at increased odds of minor complications (OR 1.22, 95%CI 1.03–1.44) and increased odds of all complications (OR 1.25, 95%CI 1.08–1.46). However, in the matched cohort there was no significant difference in the odds of experiencing major complications for black versus white women.
Table 6:
Characteristics of Propensity Score Matched Cohort Analysis
| Mean Exposed |
Mean Control |
% reduction bias | bias | t | p value | ||
|---|---|---|---|---|---|---|---|
| Open Surgical Route | Unmatched | 0.50 | 0.23 | 58.7 | 32.78 | <0.001 | |
| Matched | 0.44 | 0.45 | −1.7 | 97 | −0.66 | 0.51 | |
| Hx Abdominal Surgery | Unmatched | 0.19 | 0.29 | −22.1 | −11.43 | <0.001 | |
| Matched | 0.21 | 0.20 | 1.3 | 94 | 0.57 | 0.57 | |
| Prior Pelvic Surgery | Unmatched | 0.59 | 0.53 | 10.8 | 5.75 | <0.001 | |
| Matched | 0.58 | 0.57 | 1.1 | 90 | 0.44 | 0.66 | |
| History of Endometriosis | Unmatched | 0.10 | 0.13 | −9.3 | −4.81 | <0.001 | |
| Matched | 0.11 | 0.10 | 1.6 | 82.6 | 0.68 | 0.49 | |
| Age* | Unmatched | 44.08 | 48.13 | −39.8 | −19.95 | <0.001 | |
| Matched | 44.54 | 44.81 | −2.6 | 93.5 | −1.18 | 0.24 | |
| Charlson Deyo Score 1 | Unmatched | 0.09 | 0.08 | 3.7 | 1.98 | <0.001 | |
| Matched | 0.08 | 0.09 | −0.9 | 76.3 | −0.35 | 0.73 | |
| Charlson Deyo Score >2 | Unmatched | 0.01 | 0.01 | 0.5 | 0.30 | 0.77 | |
| Matched | 0.01 | 0.01 | −2.4 | 344.6 | −0.95 | 0.34 | |
| BMI* | Unmatched | 32.67 | 30.38 | 29.9 | 15.93 | <0.001 | |
| Matched | 32.16 | 32.07 | 1.1 | 96.2 | 0.44 | 0.66 | |
| Uterine Weight >250g | Unmatched | 0.61 | 0.26 | 75.9 | 41.67 | <0.001 | |
| Matched | 0.55 | 0.56 | −1.8 | 97.6 | −0.69 | 0.49 | |
| Other Procedures | Unmatched | 0.67 | 0.57 | 21.9 | 11.53 | 0.00 | |
| Matched | 0.66 | 0.66 | −0.9 | 96 | −0.36 | 0.72 |
Continuous variables
Discussion
Our data are concordant with prior studies that demonstrate a disparity in the route of hysterectomy for black women. These findings also support the hypothesis that there may be clinical differences between white and black women that influence surgeon’s choice of hysterectomy route, in particular uterine size. However, even after adjusting for these important differences, black women had persistently higher odds of undergoing open hysterectomy. Black women also experienced more complications when undergoing any hysterectomy, which decreased, but were not eliminated when adjusting for route of hysterectomy.
Prior investigation into complications from hysterectomy by Mehta, et al, identified that Black race was associated with higher rate of complications.21 This same analysis identified that minimally invasive hysterectomy was also associated with lower complications, however, the study did not investigate if minimally invasive hysterectomy mitigated complication rates specifically for women of black race. The findings from our analysis help to bridge this gap in knowledge. Some of the postoperative complications experienced by black women are likely attributable to the fact that black women are more likely to undergo an open hysterectomy. However, as black race is still associated with a higher odds of complications, even when adjusting for hysterectomy route, there are other contributing factors that warrant further investigation.
One possible explanation for our findings is that women of minority race might have disparate access to gynecologic care. Ranjit et al., attempted to answer this question by examining women of equivalent insurance and, therefore, presumably equal access to care. Black women still had greater odds of undergoing an open hysterectomy, however the study did not fully take into consideration patient level factors.7 In another study by Price et al, a small sample size of patients from three hospitals with high rates of minimally invasive hysterectomy found that black women did not have increased odds of having an open hysterectomy when controlling for other factors, including uterine size. 6 The findings of Price et al, suggest that access to care and quality of hospital care may be important factors to explore.
The strength of this study is the reliable, accurate database that is the source of data and which have been used to assess postoperative complications from hysterectomy and other surgical procedures for many other studies.15,22,23 The database provided data for a large sample of patients from many different hospitals and included patient-level medical information collected specifically for the use of examining postoperative outcomes. The addition of the targeted hysterectomy file within NSQIP allowed for adjustment of important patient-level factors, such as uterine size, obesity, and comorbidities, not previously available in other secondary dataset studies, yet factors that many gynecologic surgeons take into consideration in their decision-making about route of hysterectomy.
Limitations of the study include the potential for unmeasured bias. There may be other individual, system, or environmental factors that predispose black women to undergo open hysterectomy or to have more postoperative complications. Specifically, no studies about patient preference of surgeon, hospital, or route of hysterectomy have been published. Additionally, the exact hospital where each hysterectomy was performed is not available in the database. Indeed, there may be regional or geographic and practice patterns where black women are more or less likely to receive care for conditions requiring a hysterectomy. However, this study suggests that, regardless of local practice patterns, minimally invasive hysterectomy should be given greater consideration, especially when deciding the route of hysterectomy surgery for black women. Lastly, the database gives no information regarding surgeon volume or years of experience which may be important contributors to complication rates and may additionally provide insight into the physicians that are caring for black women.
Although open hysterectomy and postoperative complications are also associated, this association alone does not explain the increased odds of complications experienced by black women, as demonstrated by the findings. System-level factors may contribute to black women receiving less guideline-concordant care, and thereby, resulting in more postoperative complications necessitates further investigation. This study suggests that an important step to reduce the disparity in route of surgery and postoperative complications is to increase access to and utilization of minimally invasive surgery. However, future research needs to explore other contributing factors.
Supplementary Material
Acknowledgments
Supported by NIH K12 HD050121-12.
Footnotes
Presented at the Society for Gynecologic Oncology Annual Meeting March 24th-27th, 2018, New Orleans, LA.
Financial Disclosure
The authors did not report any potential conflicts of interest.
Each author has indicated that he or she has met the journal’s requirements for authorship.
The data used in the study are derived from a deidentified National Surgical Quality Improvement file. The American College of Surgeons have not verified and are not responsible for the analytic or statistical methodology used, or the conclusions drawn from these data by the investigators.
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