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Health Care Disparities in Hysterectomy for Gynecologic Cancers

Data From the 2012 National Inpatient Sample

Esselen, Katharine M. MD, MBA; Vitonis, Allison SM; Einarsson, Jon MD, PhD; Muto, Michael G. MD; Cohen, Sarah MD, MPH

doi: 10.1097/AOG.0000000000001088
Contents: Original Research
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OBJECTIVE: To examine hysterectomies in the United States performed for gynecologic malignancies and identify factors associated with the use of minimally invasive techniques.

METHODS: This is a cross-sectional analysis of the 2012 National Inpatient Sample, the largest national all-payer database of hospital discharges. International Classification of Diseases, 9th Revision, Clinical Modification codes for any type of hysterectomy performed for gynecologic malignancy were used to abstract pertinent observations. Weighted multivariable logistic regression models were used to examine the associations between demographic and clinical factors and mode of hysterectomy by cancer diagnosis.

RESULTS: In 2012, there were an estimated 46,450 hysterectomies for gynecologic malignancy in the United States. Of these, 28,285 (61%) were performed for uterine, 4,275 (9%) for cervical, 12,370 (27%) for ovarian cancer, and 1,520 (3%) for other gynecologic malignancies. Minimally invasive hysterectomy was used in 50% of uterine, 43% of cervical, and 8.5% of ovarian cancer cases. Black women had decreased odds of undergoing minimally invasive hysterectomy for uterine (adjusted odds ratio [OR] 0.50, 95% confidence interval [CI] 0.40–0.0.63, P<.001) and cervical (adjusted OR 0.56, 95% CI 0.33–0.96, P=.03) cancers. Those without insurance or with Medicaid had decreased odds of undergoing minimally invasive hysterectomy (P<.001) for uterine cancer. As compared with the Northeast, patients in the South (adjusted OR 0.72, 95% CI 0.53–0.98, P=.04) were less likely to undergo minimally invasive hysterectomy for uterine cancer, whereas those in the West more likely (adjusted OR 1.48, 95% CI 1.10–1.99, P=.009).

CONCLUSION: Minimally invasive hysterectomy for gynecologic malignancies remained underused in 2012; there were striking racial disparities associated with use of minimally invasive hysterectomy for uterine and cervical cancers.

LEVEL OF EVIDENCE: III

Minimally invasive hysterectomy for gynecologic malignancy remains underused, and there are striking racial disparities associated with its use in uterine and cervical cancers.

Division of Gynecologic Oncology, Department of Obstetrics and Gynecology, Brigham & Women's Hospital, Dana Farber Cancer Institute, Harvard Medical School, and the Obstetrics and Gynecology Epidemiology Center and the Division of Minimally Invasive Gynecology, Department of Obstetrics and Gynecology, Brigham & Women's Hospital, Harvard Medical School, Boston, Massachusetts.

Corresponding author: Katharine M. Esselen, MD, MBA, Division of Gynecologic Oncology, 75 Francis Street, Boston, MA 02115; e-mail: kesselen14@gmail.com.

Financial Disclosure The authors did not report any potential conflicts of interest.

Value-based health care is a health care strategy that focuses on delivering the best patient outcomes for the least cost.1 Minimally invasive techniques are an opportunity to improve the value of care delivered to patients, and as such, the application of minimally invasive hysterectomy to surgical management of gynecologic cancer has dramatically increased over the past two decades.2,32,3 Both prospective and retrospective comparisons of traditional abdominal hysterectomy with minimally invasive hysterectomy have demonstrated that it is equally safe and effective in uterine and cervical cancers with similar oncologic outcomes.4–74–74–74–7 Compared with abdominal hysterectomy, minimally invasive hysterectomy is associated with less blood loss, shorter lengths of hospital stay, and faster recovery times.4–84–84–84–84–8 Despite these advantages, certain racial or ethnic groups may be more likely to undergo abdominal surgery.9–129–129–129–12 Minorities have also been shown to have a higher risk of cancer death or suboptimal treatment in both gynecologic and nongynecologic disease.13–1513–1513–15 Specifically, studies have shown that black women with endometrial and cervical cancer have increased mortality rates and tend to present with more advanced disease.16,1716,17

The objective of this study is to provide an overview of the state of hysterectomy in the United States for gynecologic malignancies in 2012. We aim to study the mode of hysterectomy by cancer diagnosis to identify specific patient and health system factors that are associated with the use of minimally invasive techniques. Furthermore, as a first step toward evaluating the economic effects of the care we are delivering, we examine costs across all hysterectomies.

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MATERIALS AND METHODS

The National Inpatient Sample was developed as part of the Healthcare Cost and Utilization Project and is managed by the Agency for Healthcare Research and Quality. It is the largest publicly available all-payer database of inpatient care in the United States. The National Inpatient Sample approximates a 20% stratified sample of discharges from all non-Federal short-term, general and specialty hospitals, excluding rehabilitation and long-term acute care hospitals. Weighting procedures are applied to the National Inpatient Sample database to extrapolate the data to national estimates that represent approximately 95% of the U.S. population. In 2012 the National Inpatient Sample was redesigned to reduce sampling error within the database and includes data from more than 7 million hospital stays in 44 states. More detail can be found regarding the 2012 update to the National Inpatient Sample and sampling and weighting procedures on the Healthcare Cost and Utilization Project web site.18 The National Inpatient Sample has been used by researchers and policymakers to obtain national estimates of health care utilization since 1988 and specifically within the field of gynecology has allowed for examination of important population-based trends in hysterectomy.9,10,199,10,199,10,19 This study was deemed exempt by the Partners institutional review board because it did not require direct patient contact or use identifying patient information.

Using the 2012 National Inpatient Sample, we identified discharges for hysterectomy using International Classification of Diseases, 9th Revision, Clinical Modification (ICD-9-CM) codes between 68.3 and 68.99. Clinical classification software categorization was then used to identify hysterectomies performed for a gynecologic malignancy. Clinical classification software is a system by which all ICD-9-CM codes related to single diagnoses such as uterine cancer are grouped into a single entity. Thus, records were then able to be categorized into uterine, cervical, and ovarian cancer subgroups (Table 1). Of note, the cervical cancer Clinical classification software code includes ICD-9-CM codes for precancerous cervical dysplasia; thus, those were removed from the analysis, whereas the ovarian cancer Clinical classification software codes do not include fallopian tube and peritoneal cancers and those codes were added to the analysis. Hysterectomies for multiple primary diagnoses of ovarian, endometrial, or cervical cancer or “other” gynecologic cancer designation were excluded from this analysis. Within each cancer subgroup, ICD-9-CM procedure codes were used to designate the mode of hysterectomy including abdominal, vaginal, laparoscopic, and other; any case with a robotic modifier was classified as a robotic approach (Table 1). Of note, a majority of these robotic-assisted cases were colabeled as laparoscopic hysterectomies and a small number were also coded as abdominal or vaginal procedures. Although it was unclear if the cases coded as both robotic and abdominal and vaginal procedures represent conversions or are misclassified, the authors chose to treat all cases coded with modifiers for robotic assistance as a separate category of robot-assisted hysterectomy.

Table 1

Table 1

Available demographic variables included age, race (white, black, Hispanic, Asian or Pacific Islander, Native American, other), insurance type (private, Medicaid, Medicare, self-pay, no charge), and household income. Clinical variables for each hysterectomy were also collected, including other surgical diagnoses such as leiomyomas, endometriosis, prolapse, and menstrual disorders. A severity of illness subclass variable was used as a proxy for extent of comorbidities, and the Agency for Healthcare Research and Quality obesity comorbidity measure was also collected. Hospital-based information was abstracted including size of the hospital by bed size (small, medium, large), urban or rural location, hospital teaching status, and region of the country (Northeast, Midwest, South, West). Finally, total charges and hospital length of stay were collected for all hysterectomies. The National Inpatient Sample includes an estimate of the cost-to-charge ratio for each hospital and by multiplying total charges by this ratio, we estimated total costs.

Because of the sampling design, weighted analyses were carried out using the survey analysis procedures in SAS 9.2. Using these methods we calculated a national estimate for the total number of hysterectomies performed for gynecologic cancer and estimates for the each type of hysterectomy. We calculated crude and adjusted odds ratios (ORs) and 95% confidence intervals (CIs) using logistic regression analyses to estimate the associations between patient and hospital characteristics and risk of minimally invasive surgery compared with abdominal hysterectomy for each type of malignancy. Minimally invasive surgery was defined as laparoscopic, robotic, or vaginal surgery. The multivariable models included all predictor variables, but because severity of illness subclass and obesity are highly correlated and their estimates become unstable when modeled together, we constructed separate models for each of these variables. Further analyses were also performed within each cancer diagnosis to compare abdominal hysterectomy with vaginal hysterectomies and abdominal hysterectomy with laparoscopic or robotic hysterectomies. Although most variables had no or only small amounts of missing data, the race classification was missing for 6% of the sample. To prevent variables with missing values from being dropped from analyses, we assigned missing indicators and included these indicators in the regression models. Only the OR (95% CI) for the race missing indicator is shown in the results. To examine difference in total charges and costs across hysterectomy type, we first log-transformed total charges and costs to create normal distributions and ran weighted linear regression models to account for the sampling design. We performed this analysis for all cancers and for each cancer type separately.

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RESULTS

There were 9,290 hysterectomy discharges in the 2012 National Inpatient Sample, representing approximately 46,450 hysterectomies performed with an associated gynecologic malignancy diagnosis in the United States in 2012. Oncologic indications for hysterectomy included 28,285 (61%) cases for uterine cancer, 4,275 (9%) cases for cervical cancer, and 12,370 (27%) cases for ovarian cancer. The remaining 1,520 (3%) were for women with multiple primary gynecologic cancers or other gynecologic malignancies diagnoses. Figure 1 demonstrates the varying modes of hysterectomy across cancer diagnoses.

Of the estimated 28,285 hysterectomies performed for uterine cancer in the 2012 National Inpatient Sample database, 125 surgeries were either coded as pelvic evisceration or unspecified and were excluded from further analysis. Of the remaining 28,160 hysterectomies, 13,950 (50%) were abdominal and 14,210 (50%) were minimally invasive. Specifically, 10,565 (38%) were robotic, 3,240 (11%) were laparoscopic, and 405 (1%) were vaginal (Fig. 1). Urban–rural designations, median household income, and region of hospital variables were heterogeneously distributed among the four modes of hysterectomy. Medicare and private insurance including health maintenance organizations were the primary payers across all types of hysterectomy. Large bed size hospitals and urban teaching hospitals accounted for the majority of all hysterectomy procedures regardless of surgical approach. The characteristics of the uterine cancer cohort classified by mode of hysterectomy are shown in detail in Appendix 1, available online at http://links.lww.com/AOG/A702.

The multivariable regression model demonstrated that several variables were associated with the mode of hysterectomy for uterine cancer (Table 2). Compared with white patients, black (adjusted OR 0.50, 95% CI 0.40–0.0.63, P<.001) and Native American (adjusted OR 0.56, 95% CI 0.39–0.82, P=.003) races were associated with lower odds of minimally invasive hysterectomy. Compared with women with private insurance, Medicaid patients had lower odds of having a minimally invasive hysterectomy (adjusted OR 0.58, 95% CI 0.44–0.75, P<.001) as did self-pay patients (adjusted OR 0.50, 95% CI 0.34–0.72, P<.001). There were also geographic differences in the performance of minimally invasive hysterectomy. As compared with patients in the Northeast, patients in the West were more likely to undergo minimally invasive hysterectomy (adjusted OR 1.48, 95% CI 1.10–1.99, P=.009), whereas those in the South (adjusted OR 0.72, 95% CI 0.53–0.98, P=.04) were less likely to undergo a minimally invasive hysterectomy. Patients accessing care in urban teaching hospitals had the greatest odds of undergoing minimally invasive hysterectomy (adjusted OR 3.68, 95% CI 1.57–8.62, P=.003) as compared with rural hospitals. Finally, the severity of illness subclassification system that groups patients by functional status showed that with increasing loss of function, there was an increasing odds of having an abdominal procedure (all P<.001).

Table 2-a

Table 2-a

Table 2-b

Table 2-b

Total length of stay was greater than three nights for 80.1% of patients undergoing an abdominal hysterectomy for uterine cancer (Table 3). Meanwhile, laparoscopic and robotic cases were associated with only 15% of patients staying more than three nights. After vaginal hysterectomy, 25% of patients experienced a hospital stay of three or more nights. The mean total hospital costs were $15,384 for abdominal hysterectomy, $13,801 for robotic hysterectomy, $12,506 for laparoscopic hysterectomy, and $11,609 after vaginal hysterectomy for uterine cancer, with vaginal hysterectomy (P<.001) and laparoscopic hysterectomy (P<.001) associated with significantly reduced total mean costs as compared with abdominal hysterectomy (Table 4).

Table 3

Table 3

Table 4

Table 4

There were an estimated 4,275 hysterectomies performed for cervical cancer in 2012. Of those, 230 were excluded from further analysis because their surgeries were either coded as pelvic evisceration or unspecified. Of the 4,045 cases kept in the analysis, 2,320 (57%) were abdominal and 1,725 (43%) were minimally invasive. Specifically 1,085 (27%) were robotic, 465 (12%) were laparoscopic, and 175 (4%) were vaginal (Fig. 1). Private insurance including health maintenance organizations accounted for approximately half of the hysterectomies across all surgical approaches and Medicaid as the payer for another one fourth of the hysterectomies for cervical cancer. The vast majority of hysterectomies for cervical cancer occurred in urban teaching, large bed size hospitals. Appendix 2, available online at http://links.lww.com/AOG/A702, demonstrates the characteristics of the cervical cancer cohort in detail classified by mode of hysterectomy.

The multivariable regression model demonstrated that only a few variables were associated with the odds of undergoing a minimally invasive hysterectomy for treatment of cervical cancer (Table 5). Compared with white patients, black patients (adjusted OR 0.56, 95% CI 0.33–0.96, P=.03) had a lower odds of a minimally invasive hysterectomy. Self-pay patients had lower odds of minimally invasive hysterectomy (adjusted OR 0.41, 95% CI 0.18–0.89, P=.02), whereas patients with increasing median household income above $48,000 had increasing odds of minimally invasive hysterectomy (P≤.04). With regard to patient factors, there was an increasing odds of having an abdominal procedure for major to extreme loss of function (P<.001).

Table 5-a

Table 5-a

Table 5-b

Table 5-b

Total length of stay was three nights or greater for 78.8% of patients undergoing an abdominal hysterectomy for cervical cancer (Table 3). Meanwhile, the percentage of patients staying three or more nights after robotic hysterectomy, laparoscopic, or vaginal hysterectomy was 17.5%, 14%, and 28.5%, respectively. Mean total hospital costs were $14,321 for abdominal hysterectomy, $13,505 for robotic hysterectomy, $11,489 for laparoscopic hysterectomy, and $8,349 for vaginal hysterectomy for cervical cancer with only vaginal hysterectomy (P<.001) and laparoscopic hysterectomy (P=.01) demonstrating significantly decreased total mean costs as compared with abdominal hysterectomy (Table 4).

There were approximately 12,370 hysterectomies performed for ovarian cancer in 2012. Of the 12,110 surgeries analyzed after excluding 260 coded as pelvic evisceration or unspecified, 11,080 cases (91.5%) were performed abdominally and 1,030 (8.5%) through a minimally invasive approach. The characteristics of the ovarian cancer cohort by mode of hysterectomy are demonstrated Appendix 3, available online at http://links.lww.com/AOG/A702. Given that the standard of care for advanced ovarian cancer remains laparotomy and, as such, more than 90% of hysterectomies were performed abdominally for ovarian cancer in 2012, the multivariable regression comparing abdominal approach with minimally invasive approaches is not included in this report. Total length of stay was four nights or greater for 78.2% of patients undergoing abdominal hysterectomy for ovarian cancer, and mean total costs were $20,703.

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DISCUSSION

Of the greater than 30,000 hysterectomies performed in the United States in 2012 for diagnoses of uterine and cervical cancers, more than half were performed through the abdominal approach. There was increased length of stay with associated higher health care costs for the abdominal approach to hysterectomy. The most striking results of our analyses are the racial and socioeconomic disparities noted among the various modes of hysterectomy for uterine and cervical cancer. Of note, the 2012 National Inpatient Sample database does not account for procedures performed as day surgical procedures in ambulatory centers; thus, there may be a number of hysterectomies for cancer that were not captured in this analysis. However, it is likely that most hysterectomies done for gynecologic cancers in 2012 were still performed in the inpatient setting.

Our data are consistent with prior work demonstrating health care disparities along racial and socioeconomic lines; minority and lower income women have been shown to be more likely to undergo an abdominal hysterectomy for benign disease.9–129–129–129–12 Racial and socioeconomic disparities in cancer care are also pervasive. A Surveillance, Epidemiology and End Results database review of more than 2.7 million patients diagnosed with lung, breast, prostate, or colorectal cancers demonstrated that black patients had worse cancer-specific mortality and underwent definitive cancer therapy less often than white patients.20 There is a growing body of literature demonstrating inequalities in gynecologic cancer care across varying racial, ethnic, and socioeconomic strata.14–17,2114–17,2114–17,2114–17,2114–17,21

Geographic disparities were also demonstrated within the approach to hysterectomy for uterine cancer. Patients with uterine cancer had a 28% (P=.04) lower odds of a minimally invasive surgery in the South as compared with the Northeast, whereas those in the West were almost 1.5 times more likely to undergo a minimally invasive hysterectomy as compared with the Northeast (P=.003). This finding should be interpreted with caution given the inability to control for stage at presentation in this analysis. Regarding patient-specific clinical factors, women with moderate to major severity of illness had 77–82% lower odds of minimally invasive hysterectomy for uterine and cervical cancers (all P≤.002). This predominance of a maximally invasive hysterectomy for the sickest patients is counterintuitive given that these patients at highest risk for complications are being subjected to the approach associated with higher morbidity.

Health care costs as analyzed in this study encompass all care delivered during the hospitalization surrounding the hysterectomy for a gynecologic malignancy. The mean total costs for the abdominal approach were greatest for both uterine and cervical cancer diagnoses and were statistically significantly different from vaginal and laparoscopic approaches, but not from robotic surgeries despite the reduced length of stay associated with minimally invasive hysterectomy. Cost comparisons amongst the varying modes of hysterectomy have been published and demonstrate mixed results.22–3222–3222–3222–3222–3222–3222–3222–3222–3222–3222–32 Key drivers of costs across all types of hysterectomy are length of hospital stay and operative time.22 One avenue for further improvement is in further reducing length of stay, particularly because minimally invasive hysterectomy for uterine cancer is feasible as same-day discharges,33 and in 2012, approximately 40% of patients were staying two or more nights in the hospital.

Strengths of this study include the large number of patients analyzed and the variety of patient and hospital-related variables available for study. Weaknesses inherent to the use of a large national database that relies on coding data include misclassification resulting from coding error and missing data. In light of the racial disparities seen, it should be not be overlooked that there were missing data for race in 6% of this cohort. Given that the missing data are not significantly different among the varying modes of hysterectomy, any misclassification would be presumed to be nondifferential. Furthermore, we recognize that with the large number of statistical tests performed, some associations may be the result of chance. Using a simple and conservative Bonferroni correction counting each unique variable in Tables 2 and 5, our adjusted significance level would be .05/15=.003. Notably this would not alter the racial and socioeconomic associations with mode of hysterectomy in uterine cancer but may affect those seen in cervical cancer. One of the main limitations of this study design is that the National Inpatient Sample does not provide detail on stage at presentation, grade of tumor, uterine weight, or patient medical history that may affect the chosen mode of hysterectomy. The stage at presentation is a particularly important cancer-specific confounding factor that may be associated with race and certainly affects the mode of hysterectomy with more advanced stage often directing an abdominal approach for optimal cancer outcomes. Regardless, the considerable association with race and mode of hysterectomy remains significant and should prompt further investigation that examines the effects of these details not readily available in the National Inpatient Sample. Finally, use of the robotic modifier to identify robotic hysterectomies, because there is no mutually exclusive ICD-9-CM code for robotics, may lead to either over- or underreported this mode of surgery.

Our findings demonstrate that, despite the widespread acceptance of minimally invasive hysterectomy in uterine and cervical cancer diagnoses, the minimally invasive approach was underused in 2012. Moreover, marked racial and socioeconomic disparities exist in use of minimally invasive techniques in uterine and cervical cancer. It is critical to continue to monitor the surgical approach to hysterectomy for gynecologic malignancies and further study the factors that are associated with mode of hysterectomy so that we may understand these disparities and work to eradicate them. Ultimately, by expanding access to minimally invasive hysterectomy and improving its efficiency, gynecologic oncologists will be able to deliver equitable value-based health care to their patients.

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Figure

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