Social determinants of access to minimally invasive hysterectomy: reevaluating the relationship between race and route of hysterectomy for benign disease

Social determinants of access to minimally invasive hysterectomy: reevaluating the relationship between race and route of hysterectomy for benign disease

Accepted Manuscript Social determinants of access to minimally invasive hysterectomy: Re-evaluating the relationship between race and route of hystere...

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Accepted Manuscript Social determinants of access to minimally invasive hysterectomy: Re-evaluating the relationship between race and route of hysterectomy for benign disease Joan T. Price, MD MPH, Lilli D. Zimmerman, MD, Nathan C. Koelper, MPH, Mary D. Sammel, ScD, Sonya Lee, MD, Samantha F. Butts, MD MSCE PII:

S0002-9378(17)30927-4

DOI:

10.1016/j.ajog.2017.07.036

Reference:

YMOB 11791

To appear in:

American Journal of Obstetrics and Gynecology

Received Date: 14 July 2017 Revised Date:

22 July 2017

Accepted Date: 31 July 2017

Please cite this article as: Price JT, Zimmerman LD, Koelper NC, Sammel MD, Lee S, Butts SF, Social determinants of access to minimally invasive hysterectomy: Re-evaluating the relationship between race and route of hysterectomy for benign disease, American Journal of Obstetrics and Gynecology (2017), doi: 10.1016/j.ajog.2017.07.036. This is a PDF file of an unedited manuscript that has been accepted for publication. As a service to our customers we are providing this early version of the manuscript. The manuscript will undergo copyediting, typesetting, and review of the resulting proof before it is published in its final form. Please note that during the production process errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain.

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Social determinants of access to minimally invasive hysterectomy: Re-evaluating the relationship

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between race and route of hysterectomy for benign disease

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Running Title: Social Determinants of Hysterectomy Route

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Joan T PRICE MD MPH1; Lilli D ZIMMERMAN MD1; Nathan C KOELPER MPH1; Mary D

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SAMMEL ScD2; Sonya LEE MD3; Samantha F BUTTS MD MSCE1

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Medicine, Philadelphia, PA, USA

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Department of Obstetrics and Gynecology, University of Pennsylvania Perelman School of

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Biostatistics, University of Pennsylvania Perelman School of Medicine, Philadelphia, PA, USA

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Department of Biostatistics and Epidemiology, Center for Clinical Epidemiology and

Department of Gynecology, Penn Presbyterian Medical Center, Philadelphia, PA, USA

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Funding: None.

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Conflicts of interest: The authors have no conflicts of interest to report.

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16 Corresponding author:

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Joan T Price, MD MPH

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Department of Obstetrics and Gynecology, UNC-Chapel Hill Medical Center

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101 Manning Drive, Chapel Hill, NC 27514

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tel: (919) 843-9546 email: [email protected]

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Abstract word count: 374

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Manuscript word count: 2,987

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Social Determinants of Hysterectomy Route

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Demographic factors are associated with access to various types of minimally invasive

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hysterectomy independent of body mass index, parity, surgical history, and uterine size.

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Running head: Social Determinants of Hysterectomy Route

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Social Determinants of Hysterectomy Route

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BACKGROUND: Racial and socioeconomic disparities exist in access to medical and surgical

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care. Studies of national databases have demonstrated disparities in route of hysterectomy for

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benign indications, but have not been able to adjust for patient-level factors that affect surgical

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decision-making.

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OBJECTIVES: To determine whether access to minimally invasive hysterectomy for benign

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indications is differential according to race independent of the effects of relevant subject-level

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confounding factors. The secondary study objective was to determine the association between

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socioeconomic status and ethnicity and access to minimally invasive hysterectomy.

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STUDY DESIGN: A cross-sectional study evaluated factors associated with minimally invasive

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hysterectomies performed for fibroids and/or abnormal uterine bleeding between 2010 and 2013

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at three hospitals within an academic university health system in Philadelphia, Pennsylvania.

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Univariate tests of association and multivariable logistic regression identified factors

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significantly associated with minimally invasive hysterectomy compared to the odds of treatment

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with the referent approach of abdominal hysterectomy.

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RESULTS: Of 1746 hysterectomies evaluated meeting study inclusion criteria, 861 (49%) were

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performed abdominally, 248 (14%) vaginally, 310 (18%) laparoscopically and 327 (19%) were

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performed with robot assistance. In univariate analysis, African-American race (OR 0.80, 95%

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CI 0.65–0.97) and Hispanic ethnicity (OR 0.63, 95% CI 0.39–1.00) were associated with lower

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odds of any minimally invasive hysterectomy relative to abdominal hysterectomy. In analyses

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additional confounding factors, African-American race was no longer a risk factor for reduced

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minimally invasive hysterectomy (OR 0.82, 95% CI 0.61–1.10), while Hispanic ethnicity (OR

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0.45, 95% CI 0.27–0.76) and Medicaid enrollment (OR 0.59, 95% CI 0.38–0.90) were associated

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with significantly lower odds of treatment with any minimally invasive hysterectomy. In

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adjusted analyses, African-American women had nearly half the odds of receiving robot-assisted

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hysterectomy compared to whites (AOR 0.57, 95% CI 0.39-0.82), while no differences were

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noted with other hysterectomy routes. Medicaid enrollment (compared to private insurance; OR

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0.51, 95% CI 0.28–0.94) and lowest income quartile (compared to highest income quartile; OR

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0.57, 95% CI 0.38–0.85) were also associated with diminished odds of robot-assisted

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hysterectomy.

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81 CONCLUSION:

When accounting for the effect of numerous pertinent demographic and

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clinical factors, the odds of undergoing minimally invasive hysterectomy were diminished in

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women of Hispanic ethnicity and in those enrolled in Medicaid but were not discrepant along

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racial lines. However, both racial and socioeconomic disparities were observed with respect to

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access to robot-assisted hysterectomy despite the availability of robotic assistance in all hospitals

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treating the study population. Strategies to ensure equal access to all minimally invasive routes

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for all women should be explored to align delivery of care with the evidence supporting the

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broad implementation of these procedures as safe, cost effective, and highly acceptable to

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patients.

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Social Determinants of Hysterectomy Route

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Minimally invasive hysterectomy (MIH) has advantages over abdominal hysterectomy including

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shorter hospital stay, improved postoperative pain, fewer complications and lower hospital

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costs.1 The American College of Obstetrics and Gynecology encourages the application of MIH,

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particularly vaginal hysterectomy, as safer and more cost effective than abdominal surgery for

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benign indications.2 Despite established advantages of MIH, racial and socioeconomic disparities

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exist in access to these approaches.3 The disparate application of minimally invasive procedures

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among African Americans and socioeconomically disadvantaged groups has been noted across

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many surgical specialties, including gynecologic surgery.4-7 National investigations of disparities

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in MIH have found that younger age, white race, higher income and private insurance

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independently predict laparoscopic over abdominal hysterectomy.8-11

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The primary aim of this study was to determine the association between race and the odds of

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MIH for the treatment of fibroids, adenomyosis and abnormal bleeding. The secondary objective

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was to assess the relationship between indicators of socioeconomic status, ethnicity and the odds

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of MIH for the above indications. To build on findings from previous reports using national

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databases, we sought to evaluate subject-level data related to hysterectomies performed at three

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urban University-affiliated hospitals to more thoroughly control for confounding. Because

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national databases often do not differentiate between traditional laparoscopic versus robot-

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assisted routes of hysterectomy, we sought to determine whether certain individual minimally

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invasive routes were more prone to racial and/or socioeconomic disparities in sub-group

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analyses. Our hypothesis was that non-white race and low socioeconomic status would be

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associated with diminished utilization of MIH despite adjusting for confounding due to patient-

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level clinical predictors of route of hysterectomy. Elucidating disparities in access to the

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recommended hysterectomy approaches is a critical step in improving equity and optimizing

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outcomes for all women who require major gynecological surgery.

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A cross-sectional study analyzed data from subjects receiving care at the three academic

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hospitals within the University of Pennsylvania Health System (UPHS) in Philadelphia. Data

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were gathered on all hysterectomies performed for fibroids, adenomyosis and/or abnormal

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uterine bleeding at the Hospital of the University of Pennsylvania (HUP), Pennsylvania Hospital

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(PAH) and Penn Presbyterian Medical Center (PPMC) from January 2010 through December

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2013. As medical centers within an urban academic health system, each hospital has the

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resources to perform abdominal, vaginal, laparoscopic, and robot-assisted hysterectomy. The

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gynecology practice at PPMC is a two-provider high-volume private specialty practice whereas

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the HUP and PAH sites comprise multiple practice types including private generalist, academic

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sub-specialist and resident clinic practices that all perform hysterectomies for benign indications.

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Subjects who underwent abdominal, vaginal, laparoscopic and robot-assisted hysterectomy for

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abnormal uterine bleeding, adenomyosis or fibroids were identified using diagnosis and

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procedure codes from the International Classification of Disease, Ninth Revision, Clinical

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Modification (ICD-9-CM). Exclusion criteria were: presence of known or suspected cancer,

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known endometriosis, and cases performed jointly with another surgical service. Using reports

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from the Penn Data Store clinical database and verified by electronic medical record review,

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patient-level data were collected on demographic information, primary indication and mode of

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code of residence),12 and insurance. Insurance status was categorized as (1) private insurance, (2)

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health maintenance organization / preferred provider organization (HMO/PPO), which

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comprised only non-Medicaid, non-Medicare managed plans; (3) Medicaid (including managed

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Medicaid); (4) Medicare (including managed Medicare); and (5) self-pay or uninsured. Both

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uterine weight and volume were abstracted from surgical pathology reports for each subject. The

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final multivariable analyses adjusted only for uterine weight to avoid colinearity by including

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both variables. Uterine weight was chosen as the more objective measure; volume estimates can

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be imprecise when fibroids distort the uterine contour.

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The primary study outcome was mode of hysterectomy. Any abdominal hysterectomy including

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total abdominal and abdominal supracervical hysterectomy was placed in the “abdominal”

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category. Total vaginal hysterectomy without laparoscopic assistance was its own category

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whereas

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hysterectomy was coded as “laparoscopic”. In cases performed with robot assistance, the

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hysterectomy was categorized as “robotic”. Hysterectomies were categorized under the initial

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route of hysterectomy regardless of intra-operative conversion in order to reflect pre-operative

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decision-making and surgical planning.

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laparoscopic-assisted,

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any

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Continuous variables were summarized using means and standard deviations, while frequencies

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were used to describe the categorical variables. Age, BMI, uterine weight, and uterine volume

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were treated as continuous variables. Uterine weight was transformed into a categorical variable

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based on contingency tables detecting a frequency of at least two individuals in cross tabulation.

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Univariate comparisons of each of the potential predictors were performed with the dichotomous

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outcomes of abdominal versus all MIH, vaginal, laparoscopic, and robotic hysterectomy, using

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Pearson’s chi-square tests, Student’s t-tests or simple logistic regression as appropriate.

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Four logistic regression models were fit to determine the set of independent variables that best

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predicted the odds of abdominal compared to any MIH, vaginal, laparoscopic, or robotic

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hysterectomy. Backward selection was used to generate final models starting with all variables of

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interest then excluding those that were not significant and successively re-fitting reduced models

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until all remaining variables were statistically significant at p<0.05. Variables associated with

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slightly higher p values (p<0.5) were retained if they were known risk factors for abdominal

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hysterectomy or if the effect estimate for race changed by >10% when the covariate was

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removed. Likelihood ratio testing was used to screen the robustness of covariates to generate a

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parsimonious final model and to test for the presence of interactions. Statistical analyses were

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performed using SAS 9.3 statistical software, Cary, NC.

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The University of Pennsylvania Institutional Review Board granted approval to conduct this

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study prior to the commencement of data collection; the requirement for informed consent was

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waived.

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RESULTS

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A total of 2166 hysterectomies were performed for the indications of fibroids, adenomyosis

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and/or abnormal uterine bleeding at three UPHS hospitals between January 1, 2010 and

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December 31, 2013. Of these cases, 420 (19%) were excluded, generating a sample of 1746

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eligible cases for analysis (Figure 1). Missing data were rare and addressed using listwise

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deletion.

185 Most participants self-identified as either African American (57%, n=978) or white (38%,

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n=659) (Table 1). More than half (55%) resided in zip codes representing neighborhoods in the

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two lowest median household income quartiles (<$48,000 annually). Most subjects were covered

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by either private insurance (35%) or managed care (50%).

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Among 1746 hysterectomies, 49% (N=861) were performed abdominally, 14% (N=248)

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vaginally and 37% (N=637) laparoscopically (Table 1). Of the laparoscopic hysterectomies, 327

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(19% of total) were performed with robotic assistance. The primary indication for hysterectomy

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was fibroids for 80% of participants.

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Most white subjects (54%) underwent MIH; more than half of those (28% overall) were

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performed with robotic assistance. Among African-American women, 48% underwent MIH;

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only 25% of those (12% overall) were robot-assisted. The proportion of whites treated with

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vaginal hysterectomy was 9% while 18% of African Americans had hysterectomy performed

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vaginally. Most vaginal hysterectomies (71%) were performed in African Americans.

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Examining the association of race and other clinical or demographic variables revealed that

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African-American women were slightly younger (p<.001) with modestly higher BMIs compared

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to white women (p<.001; Table 2). More African-American women than white women had

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fibroids as their primary diagnosis (p<.001), had surgery performed at PPMC (p<.001), were in

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the lower income quartiles (p<.001), were covered by Medicaid (<.001), had a prior vaginal

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delivery (p<.001), had a prior abdominal surgery (p=.005), and had larger uteri by both weight

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and volume (p<.001).

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Univariate analysis demonstrated relationships between route of hysterectomy and race,

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ethnicity, insurance status, and median household income quartile (Table 3). Comparing

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abdominal hysterectomy to all minimally invasive routes combined, African-American patients

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had lower odds of undergoing MIH than whites (OR 0.80, 95% CI 0.65–0.97), an association

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that achieved borderline significance. African Americans had even lower odds than whites when

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comparing robot-assisted hysterectomy alone to abdominal hysterectomy (OR 0.38, 95% CI

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0.29–0.50). Conversely, African Americans had greater odds than whites of undergoing a vaginal

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hysterectomy compared to abdominal hysterectomy (OR 1.67, 95% CI 1.21-2.30).

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Neither household income quartile nor insurance status was associated with MIH over abdominal

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hysterectomy in univariate analyses. However, women with Medicaid had significantly lower

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odds of undergoing robot-assisted than abdominal hysterectomy (OR 0.45, 95% CI 0.24–0.86)

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when compared to women with private insurance. Similarly, women in the lowest median

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household income quartile had lower odds of treatment with robot-assisted hysterectomy (OR

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0.35, 95% CI 0.25–0.49) compared to those residing in the highest quartile. Conversely, when

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compared to those in the highest income quartile, women in the lowest quartile had higher odds

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of vaginal hysterectomy than abdominal hysterectomy (OR 2.51, 95% CI 1.70–3.69).

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ACCEPTED MANUSCRIPT Price 11 In multivariable logistic regression models, we found that adjusting for subject-level factors

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mitigated many of the univariate associations between route of hysterectomy and race, ethnicity,

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median household income quartile, and insurance status (Table 4). When compared to white

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women, African-American women had similar odds of undergoing any mode of MIH as they did

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abdominal hysterectomy (AOR 0.82; 95% CI 0.61–1.10). In a subgroup multivariable analysis

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investigating the robot-assisted route alone as the alternate to abdominal hysterectomy, African-

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American women had significantly lower odds of robot-assisted hysterectomy compared to

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whites (AOR 0.57, CI 0.39–0.82). Racial disparities in vaginal and laparoscopic hysterectomy

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compared to abdominal hysterectomy were not statistically significant in adjusted analyses.

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Compared to women of non-Hispanic ethnicity, self-identified Hispanic women had lower

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adjusted odds of all MIH (AOR 0.45, 95% CI 0.27–0.76), which was predominantly driven by

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significantly lower odds of both vaginal (AOR 0.24, 95% CI 0.09–0.64) and laparoscopic

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hysterectomy (AOR 0.42, 95% CI 0.20–0.89), but not robotic hysterectomy.

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Median household income quartile and insurance coverage modestly predicted mode of

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hysterectomy in multivariable regression. In the primary analysis, income quartile did not

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predict MIH over abdominal hysterectomy, but women with Medicaid had significantly lower

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odds of MIH compared to women with private insurance (AOR 0.59, 95% CI 0.38–0.90). In

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separate subgroup analyses, women in the lowest income quartile (AOR 0.57, 95% CI 0.38–

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0.85) or with Medicaid (AOR 0.51, 95% CI 0.28–0.94) both had nearly half the odds of robot-

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assisted over abdominal hysterectomy than women in the highest income quartile or those with

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private insurance, respectively. Conversely, women in the lowest income quartile had

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significantly greater odds of undergoing vaginal over abdominal hysterectomy than those in the

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highest quartile (AOR 2.52, 95% CI 1.51–4.21). Insurance status did not modify the association

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between African-American race and mode of hysterectomy described in the multivariable

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models.

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Our analysis demonstrates that racial and socioeconomic disparities in the application of

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minimally invasive hysterectomy to treat benign gynecological disorders may be mitigated by

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adjusting for patient-level confounding factors. In contrast to national registry studies, our

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findings demonstrate that African-American women requiring hysterectomy for fibroids and/or

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abnormal bleeding had similar odds as white women of treatment with MIH when controlling for

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BMI, obstetrical and surgical history, and uterine size. By generating multivariable models that

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adjusted for patient-level factors, we were able to expose the role of confounding on previously

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described associations between race and access to MIH.4,8-11

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In the United States; African-American race, low income, and underinsurance are all associated

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with overweight and obesity.13 Obesity limits the application of laparoscopic and robot-assisted

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surgery; obese women have greater odds of vaginal over other routes of hysterectomy.14

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Similarly, fibroids disproportionately affect African-American women, who have both larger and

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more numerous fibroids than whites.15-17 In our analysis, controlling for confounding due to BMI

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and uterine weight certainly reduced the magnitude and significance of racial disparities noted in

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unadjusted analyses. However, sensitivity analyses limited to procedures performed among

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women with uterine weights <400g did not alter the findings of the remaining racial and

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socioeconomic disparities in access to robotic hysterectomy. Large national databases often do

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not report BMI or uterine size such that previous analyses of nationwide disparities in mode of

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hysterectomy have not been able to account for their effect on surgical route.3,4,8-11

276 In our study population, disparities in access to MIH due to insurance and income status are less

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stark than in national analyses, given the ability to more comprehensively address confounding

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due to multiple factors. By using data from three hospitals within one urban hospital system in

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Philadelphia, our analysis among a relatively uniform population may have biased some

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socioeconomic associations towards the null. The small proportion of patients covered by

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Medicaid in our sample could be due to the evolving composition of insurance provider types in

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an era marked by insurance reforms under the Affordable Care Act. Improving insurance

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coverage for nonwhite patients in states like Massachusetts has been met with near complete

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resolution of racial disparities in minimally invasive surgeries.18 Similarly, in an urban setting

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such as Philadelphia where neighborhoods and zip codes are more economically diverse than in

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suburban and rural communities, median household income quartile based on zip code of

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residence is likely an imperfect proxy for individual socioeconomic status. Unfortunately,

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specific individual economic productivity data were not available for query in our medical

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system’s database. Despite these limitations, we still observed that having private insurance

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(compared to Medicaid) was independently associated with greater access to MIH. Being in the

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highest income quartile (compared to the lowest) and having private insurance (compared to

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Medicaid) also predicted robot-assisted hysterectomy over abdominal hysterectomy in adjusted

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subgroup analyses. These findings are comparable to national reports that did not control for

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subject-level confounding.3,4,8-11

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ACCEPTED MANUSCRIPT Price 14 Previous analyses have shown racial and socioeconomic disparities in laparoscopic hysterectomy

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overall but most have not evaluated the role of robot-assisted hysterectomy specifically, as

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national databases rarely differentiate between laparoscopic surgeries performed with and

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without robot assistance.4,8-11 In our subgroup analyses, adjusting for confounding in

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multivariable analysis did eliminate many univariate associations between sociodemographic

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factors and the outcome of MIH versus abdominal hysterectomy. In specifically investigating

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robot-assisted hysterectomy, however, we found racial and economic disparities not apparent in

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other MIH routes, even despite controlling for patient-level factors. The ability to test specific

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associations that apply to discrete categories of MIH is a unique feature of this investigation. It is

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plausible that, as a more established and cost-effective route when compared to robot-assisted

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surgery,19,20 laparoscopic hysterectomy is more equally accessible – both regionally and across

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diverse communities. The divergent associations of race and income on different modes of MIH

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may explain why the combined outcome of MIH overall failed to demonstrate significant

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disparity and supports the investigation of laparoscopic and robot-assisted hysterectomies

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separately.

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In contrast to trends in robot-assisted hysterectomy, the odds of undergoing vaginal

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hysterectomy over abdominal hysterectomy were higher among women in the lowest income

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quartile compared to those in the highest income quartile and among African Americans

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compared to whites. Individual practice patterns and patient characteristics at the three hospitals

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could explain the findings noted despite having controlled for hospital itself. It is conceivable

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that the individual practices of the highest-volume surgeons at each hospital influenced our

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findings. At PPMC, vaginal and laparoscopic hysterectomies are exceedingly more common than

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income and African American than at the other two hospitals. Restricting the analysis to PAH

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and HUP did not alter the magnitude or significance of the associations with robot-assisted

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compared to abdominal hysterectomy, but did further increase the odds of vaginal hysterectomy

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among women in the lowest compared to highest income quartile. The differential application of

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vaginal hysterectomy over abdominal hysterectomy to low-income women may be due to

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employment status, less lenient work or childcare schedules, and other economic considerations,

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which may not only favor vaginal over abdominal hysterectomy, but may also influence the

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initial decision to perform hysterectomy over more conservative management.21-23 Overall,

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vaginal hysterectomy trends within our health system appear to be mitigating rather than

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potentiating disparities apparent in other minimally invasive routes.

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Although efforts to decrease the proportion of hysterectomies performed abdominally are

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improving uptake of MIH overall, understanding and minimizing factors that may perpetuate

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racial and socioeconomic inequities must be prioritized locally and nationally, particularly as

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vaginal hysterectomies become increasingly rare and robot-assisted hysterectomies become

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increasingly common.24,25 Vaginal hysterectomy is the preferred route for all patients for whom

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it is feasible and safe, yet the proportion of hysterectomies performed vaginally remains low in

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our population and nationwide.1,2 Gynecological training programs should continue to teach

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vaginal hysterectomy as a low-cost minimally invasive approach that may also promote a more

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equitable application of MIH to all women.2

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ACCEPTED MANUSCRIPT Price 16 This analysis has limitations. Despite the large, diverse, well-characterized cohort studied, the

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data represent a retrospective analysis and uncontrolled confounding may exist. We chose to

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exclude hysterectomies performed with known or suspected endometriosis due to the effect

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adhesive disease can have on surgical decision-making. While this may limit the generalization

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of our analysis, most benign hysterectomies in the United States are performed for fibroids or

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abnormal bleeding.26 Similarly, the generalizability of our findings does not extend to other

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hospital systems in other geographic locations and controlling for individual providers or

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provider characteristics within our study was beyond the scope of our analysis. Future research

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that purposefully selects a robust pool of data from hospitals across the country with diverse

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patients, providers, and practice types could address confounding factors of both patients and

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providers to better address these limitations.

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Our sub-regional analysis of racial and socioeconomic disparities in route of hysterectomy for

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benign indications suggests that disparities reported in national analyses may be due to

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uncontrolled patient-level confounding factors that influence surgical decision-making. We must

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interpret national analyses of disparities with caution as we have shown that adjusting for

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patient-level factors can mitigate and even eliminate associations found in unadjusted analyses.

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Still, the persistence of some disparities in access to MIH approaches despite controlling for

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multiple confounding factors remains a concern. The repeated publication of data revealing

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racial and socioeconomic disparities in medical and surgical care demands a multidisciplinary

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effort to carefully elucidate the source and true extent of these inequities, and collaborative

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strategies to ensure equitable access to all modes of MIH for racial minorities, the underinsured,

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and low-income women.

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Acknowledgements: The authors would like to thank the Penn Data Store for assistance in

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assembling information used in this study. We thank Dr. Robert L. Dood for his contribution to

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preliminary data analysis.

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REFERENCES

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Aarts JW, Nieboer TE, Johnson N, et al. Surgical approach to hysterectomy for benign gynaecological disease. Cochrane Database Syst Rev. 2015;8:CD003677. ACOG Committee Opinion No. 444: choosing the route of hysterectomy for benign disease. Obstet Gynecol. 2009;114(5):1156-1158. Abenhaim HA, Azziz R, Hu J, Bartolucci A, Tulandi T. Socioeconomic and racial predictors of undergoing laparoscopic hysterectomy for selected benign diseases: analysis of 341487 hysterectomies. J Minim Invasive Gynecol. 2008;15(1):11-15. Jacoby VL, Autry A, Jacobson G, Domush R, Nakagawa S, Jacoby A. Nationwide use of laparoscopic hysterectomy compared with abdominal and vaginal approaches. Obstet Gynecol. 2009;114(5):1041-1048. Varela JE, Nguyen NT. Disparities in access to basic laparoscopic surgery at U.S. academic medical centers. Surg Endosc. 2011;25(4):1209-1214. Robinson CN, Balentine CJ, Sansgiry S, Berger DH. Disparities in the use of minimally invasive surgery for colorectal disease. J Gastrointest Surg. 2012;16(5):897-903; discussion 903-894. Trinh QD, Schmitges J, Sun M, et al. Improvement of racial disparities with respect to the utilization of minimally invasive radical prostatectomy in the United States. Cancer. 2012;118(7):1894-1900. Esselen KM, Vitonis A, Einarsson J, Muto MG, Cohen S. Health Care Disparities in Hysterectomy for Gynecologic Cancers: Data From the 2012 National Inpatient Sample. Obstet Gynecol. 2015;126(5):1029-1039. Lee J, Jennings K, Borahay MA, et al. Trends in the national distribution of laparoscopic hysterectomies from 2003 to 2010. J Minim Invasive Gynecol. 2014;21(4):656-661. Patel PR, Lee J, Rodriguez AM, et al. Disparities in use of laparoscopic hysterectomies: a nationwide analysis. J Minim Invasive Gynecol. 2014;21(2):223-227. Price JT, Lee S. National Trends and Disparities in Minimally Invasive Approaches to Hysterectomy for Benign Indications. Journal of Minimally Invasive Gynecology. 20(6):S11-S12. American Community Survey, 2013 American Community Survey 3-year estimates, Table B19013. http://factfinder2.census.gov. Ogden CLCL. Prevalence of childhood and adult obesity in the United States, 2011-2012. JAMA : the journal of the American Medical Association.311(8):806. Mikhail E, Miladinovic B, Velanovich V, Finan MA, Hart S, Imudia AN. Association between obesity and the trends of routes of hysterectomy performed for benign indications. Obstet Gynecol. 2015;125(4):912-918. Eltoukhi HM, Modi MN, Weston M, Armstrong AY, Stewart EA. The health disparities of uterine fibroid tumors for African American women: a public health issue. Am J Obstet Gynecol. 2014;210(3):194-199. Baird DD, Dunson DB, Hill MC, Cousins D, Schectman JM. High cumulative incidence of uterine leiomyoma in black and white women: ultrasound evidence. Am J Obstet Gynecol. 2003;188(1):100-107. Moore AB, Flake GP, Swartz CD, et al. Association of race, age and body mass index with gross pathology of uterine fibroids. J Reprod Med. 2008;53(2):90-96.

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21. 22. 23. 24. 25. 26.

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Loehrer AP, Song Z, Auchincloss HG, Hutter MM. Massachusetts health care reform and reduced racial disparities in minimally invasive surgery. JAMA Surg. 2013;148(12):11161122. Wright JD, Ananth CV, Lewin SN, et al. Robotically assisted vs laparoscopic hysterectomy among women with benign gynecologic disease. JAMA. 2013;309(7):689698. Pasic RP, Rizzo JA, Fang H, Ross S, Moore M, Gunnarsson C. Comparing robot-assisted with conventional laparoscopic hysterectomy: impact on cost and clinical outcomes. J Minim Invasive Gynecol. 2010;17(6):730-738. Marks NF, Shinberg DS. Socioeconomic differences in hysterectomy: the Wisconsin Longitudinal Study. Am J Public Health. 1997;87(9):1507-1514. Materia E, Rossi L, Spadea T, et al. Hysterectomy and socioeconomic position in Rome, Italy. J Epidemiol Community Health. 2002;56(6):461-465. Dharmalingam A, Pool I, Dickson J. Biosocial determinants of hysterectomy in New Zealand. Am J Public Health. 2000;90(9):1455-1458. Committee on Gynecologic P. Committee Opinion No 701: Choosing the Route of Hysterectomy for Benign Disease. Obstet Gynecol. 2017;129(6):e155-e159. Wright JD, Herzog TJ, Tsui J, et al. Nationwide trends in the performance of inpatient hysterectomy in the United States. Obstet Gynecol. 2013;122(2 Pt 1):233-241. Kho KA, Lin K, Hechanova M, Richardson DL. Risk of Occult Uterine Sarcoma in Women Undergoing Hysterectomy for Benign Indications. Obstet Gynecol. 2016;127(3):468-473. Shirlina D, Shirish S. Uterine volume: an aid to determine the route and technique of hysterectomy. J Obstet Gynecol Ind. 2004;54(1):68-72.

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Table 1. Baseline Characteristics of 1746 women who underwent hysterectomy for benign indications, 2010-2013 Abdominal

Vaginal

Mean (±SD)

Mean (±SD)

Mean (±SD)

or % (N)*

or % (N)*

or % (N)*

Total

100 (1746)

49 (861)

14 (248)

Age, y

45.9 (±7.2)

46.3 (±6.7)

BMI, kg/m²

30.4 (±7.2)

30.4 (±7.3)

1 (23)

0 (2)

Missing

or % (N)*

or % (N)*

18 (310)

19 (327)

44.8 (±8.0)

45.1 (±7.2)

46.6 (±7.9)

31.9 (±7.6)

30.3 (±7.0)

29.7 (±6.9)

2 (6)

2 (5)

3 (10)

M AN U

SC

Mean (±SD)

EP

Diagnosis

Mean (±SD)

TE D

Characteristic

Laparoscopic Robot-assisted

RI PT

All

AC C

Bleeding or Adenomyosis

20 (356)

13 (113)

34 (84)

25 (77)

25 (82)

Fibroids

80 (1390)

87 (748)

66 (164)

75 (233)

75 (245)

Social Determinants of Hysterectomy Route

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2010

25 (444)

26 (227)

23 (56)

2011

27 (464)

28 (242)

26 (64)

2012

26 (459)

25 (211)

28 (69)

RI PT

Year of Surgery

2013

22 (379)

21 (181)

24 (59)

HUP

40 (699)

39 (339)

PAH

46 (802)

PPMC

14 (245)

20 (65)

22 (68)

28 (90)

24 (74)

32 (105)

23 (72)

21 (67)

28 (70)

47 (146)

44 (144)

58 (502)

25 (63)

18 (56)

55 (181)

2 (20)

46 (115)

35 (108)

1 (2)

M AN U

EP

TE D

Hospital

SC

31 (96)

AC C

Race White

38 (659)

35 (303)

25 (62)

36 (111)

56 (183)

AA

56 (978)

59 (505)

69 (172)

59 (184)

36 (117)

4 (75)

4 (38)

3 (7)

3 (10)

6 (20)

Other

Social Determinants of Hysterectomy Route

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2 (34)

2 (15)

3 (7)

2 (5)

2 (7)

95 (1666)

95 (812)

98 (242)

97 (300)

95 (312)

Hispanic

5 (78)

5 (47)

2 (6)

RI PT

Price 22 Missing

3 (10)

5 (15)

Missing

0 (2)

0 (2)

0 (0)

0 (0)

0 (0)

$64,000+

31 (539)

30 (259)

16 (40)

30 (92)

45 (148)

$48-63,999

14 (239)

13 (113)

13 (31)

13 (41)

17 (54)

$38-47,999

15 (268)

15 (132)

15 (37)

14 (45)

17 (54)

$1-37,999

40 (694)

41 (354)

55 (137)

43 (132)

22 (71)

0 (3)

1 (3)

0 (0)

0 (0)

37 (318)

37 (91)

33 (102)

32 (103)

Insurance Private

EP

0 (6)

AC C

Missing

TE D

Income Quartile

M AN U

Not Hispanic

SC

Ethnicity

35 (614)

Social Determinants of Hysterectomy Route

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49 (862)

47 (403)

42 (105)

53 (163)

58 (191)

Medicaid

8 (140)

10 (82)

11 (27)

6 (19)

4 (12)

Medicare

6 (112)

6 (54)

8 (20)

7 (23)

5 (15)

Missing/Self-pay

1 (18)

0 (4)

2 (5)

1 (3)

2 (6)

Delivery

1.5 (±1.4)

1.3 (±1.4)

2.2 (±1.6)

1.6 (±1.5)

1.3 (±1.4)

0

34 (597)

39 (339)

18 (45)

30 (93)

37 (120)

1-2

42 (742)

41 (356)

40 (98)

45 (141)

45 (147)

3-4

19 (331)

16 (136)

34 (84)

18 (56)

17 (55)

≥5

4 (52)

2 (19)

6 (15)

5 (14)

1 (4)

Missing

1 (24)

1 (11)

2 (6)

2 (6)

0 (1)

SC

HMO/PPO

RI PT

Price 23

TE D

EP

AC C

Prior Cesarean

M AN U

Prior Vaginal

Delivery

0.4 (±0.8)

0.4 (±0.8)

0.2 (±0.6)

0.4 (±0.7)

0.6(±0.9)

0

74 (1298)

75 (644)

85 (210)

74 (229)

66 (215)

Social Determinants of Hysterectomy Route

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14 (240)

14 (118)

8 (21)

15 (46)

17 (55)

2

8 (139)

7 (63)

3 (8)

8 (24)

13 (44)

≥3

3 (48)

3 (27)

2 (4)

2 (5)

4 (12)

Missing

1 (21)

1 (9)

2 (5)

2 (6)

0 (1)

56 (974)

54 (467)

59 (147)

60 (185)

53 (175)

1 (16)

1 (9)

1 (2)

1 (4)

0 (1)

Uterine weight (g)

497 (±610)

716 (±775)

237 (±148)

315 (±299)

288 (±219)

Uterine volume§

579 (±882)

781 (±1057)

316 (±364)

526 (±906)

290 (±292)

SC

1

RI PT

Price 24

TE D

Missing

EP

surgery

M AN U

Prior abdominal

AC C

HUP, Hospital of the University of Pennsylvania; PAH, Pennsylvania Hospital; PPMC, Penn Presbyterian Medical Center; AA, African American; Income Quartile, median household income quartile; HMO/PPO, health maintenance organization/preferred provider organization. * Column totals may not add to 100 percent due to rounding.

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Price 25 Uterine Volume, cm³, calculated using the prolate ellipsoid formula of 4/3 x pi x L/2 x W/2 x AP/2 27

AC C

EP

TE D

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SC

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§

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438

ACCEPTED MANUSCRIPT Price 26 Table 2. Clinical and demographic variables according to race White*

AA*

Other*

% or mean

% or mean

% or mean

(±SD)

(±SD)

(±SD)

p

AA vs.

Characteristic

(N=659)

(N=978)

(N=75)

Overall

White

Age (y)

47 (±7)

45 (±7)

46 (±9)

<0.001

<0.001

BMI (kg/m²)

28 (±7)

32 (±7)

27 (±6)

<0.001

<0.001

<0.001

<0.001

0.080

0.370

<0.001

<0.001

<0.001

<0.001

Bleeding or Adenomyosis

26

Fibroids

73

RI PT

85

72

25

15

28

25

32

25

27

28

20

22

25

HUP

44

37

52

PAH

48

45

37

PPMC

7

19

11

59

10

55

2011 2012 2013

AC C

Hospital



SC 28

27

EP

2010

15

TE D

Year of Surgery

M AN U

Diagnosis



p

Income Quartile $64,000+

Social Determinants of Hysterectomy Route

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$48-63,999

17

11

16

$38-47,999

11

18

9

$1-37,999

12

61

19

Private

33

36

35

HMO/PPO

55

45

57

Medicaid

4

11

4

Medicare

6

7

Missing/Self-pay

2

1

Prior cesarean delivery

26

Prior abdominal surgery

Uterine volume (cm³)

0

59

51

0.018

<0.001

23

27

0.366

0.274

52

59

47

<0.001

0.005

407 (±555)

562 (±647)

460 (±462)

<0.001

<0.001

668 (±905)

726 (±1652)

<0.001

<0.001

EP

Uterine weight (g)

<0.001

4

M AN U

59

TE D

Prior vaginal delivery

<0.001

SC

Insurance

RI PT

Price 27

430 (±690)

AC C

AA, African American; HUP, Hospital of the University of Pennsylvania; PAH, Pennsylvania Hospital; PPMC, Penn Presbyterian Medical Center; Income Quartile, median household income quartile; HMO/PPO, health maintenance organization/preferred provider organization. *Column totals may not add to 100 percent due to rounding †

Tests of significance determined by Pearson’s chi-square for categorical and Type III ANOVA for

continuous variables

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Price 28 Table 3. Univariate analyses of race, ethnicity and socioeconomic status on minimally invasive route of hysterectomy versus

All MIH* Variable

Vaginal p‡

OR (95% CI)

OR (95% CI)

p‡

OR (95% CI)

--

Robot-assisted p‡

--

M AN U

--

Laparoscopic

SC

Race White

RI PT

abdominal hysterectomy

OR (95% CI)

p‡

--

0.80 (0.65-0.97)

0.025

1.67 (1.21-2.30)

0.002

0.99 (0.76-1.31)

0.969

0.38 (0.29-0.50) <0.001

Other

0.83 (0.51-1.34)

0.441

0.90 (0.38-2.11)

0.807

0.72 (0.35-1.49)

0.362

0.87 (0.49-1.54)

Ethnicity

0.63 (0.39-1.00)

Income Quartile $64,000+ $48-63,999

--

--

0.049

0.43 (0.18-1.01)

EP

Hispanic

--

AC C

Not Hispanic

TE D

AA

1.03 (0.76-1.40)

0.842

Social Determinants of Hysterectomy Route

-0.054

--

1.78 (1.06-2.98)

0.58 (0.29-1.15)

-0.120

-0.032

1.02 (0.66-1.57)

0.635

0.83 (0.46-1.51)

0.541

-0.923

0.84 (0.57-1.23)

0.357

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Price 29 0.95 (0.71-1.28)

0.748

1.82 (1.11-2.97)

0.019

0.96 (0.63-1.45)

0.845

0.72 (0.49-1.04)

$1-37,999

0.89 (0.71-1.11)

0.303

2.51 (1.70-3.69)

<0.001 1.05 (0.77-1.43)

0.759

0.35 (0.25-0.49) <0.001

RI PT

$38-47,999

Insurance --

--

--

SC

Private

0.76 (0.52-1.10)

0.146

1.15 (0.70-1.89)

0.580

Medicare

1.15 (0.77-1.73)

0.486

1.29 (0.70-1.89)

0.376

HMO/PPO

1.22 (1.00-1.51)

0.056

0.91 (0.74-2.27)

0.562

-0.233

0.45 (0.24-0.86)

0.010

1.33 (0.78-2.27)

0.307

0.86 (0.46-1.58)

0.620

1.26 (0.95-1.68)

0.113

1.46 (1.10-1.94)

0.007

0.72 (0.42-1.25)

M AN U

Medicaid

0.078

MIH, minimally invasive hysterectomy; OR, odds ratio; CI, confidence interval; HUP, Hospital of the University of Pennsylvania;

TE D

PAH, Pennsylvania Hospital; PPMC, Penn Presbyterian Medical Center; AA, African American; Income Quartile, median household income quartile; HMO/PPO, health maintenance organization/preferred provider organization.

Tests of significance based on Pearson's Chi-square tests

AC C



EP

*All MIH includes vaginal, laparoscopic, and robot-assisted hysterectomies

Social Determinants of Hysterectomy Route

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versus abdominal hysterectomy Vaginal

AOR†

95% CI

AOR†

--

--

--

AA

0.82

0.61-1.10

Other

0.90

Variable

95% CI

95% CI

--

--

1.38

0.86-2.21

1.06

0.73-1.56

0.57

0.39-0.82

0.52-1.56

1.65

0.58-4.68

0.99

0.45-2.15

0.82

0.43-1.58

--

--

--

--

--

--

--

--

0.45

0.27-0.76

0.24

0.09-0.64

0.42

0.20-0.89

0.78

0.39-1.53

--

--

--

--

--

TE D

--

Income Quartile $64,000+

AOR†

AC C

Hispanic

95% CI

--

Ethnicity Not Hispanic

Robot-assisted

--

EP

White

AOR†

M AN U

Race

Laparoscopic

SC

All MIH*

RI PT

Table 4. Multivariable logistic regression analysis of race, ethnicity and socioeconomic status on minimally invasive

--

--

Social Determinants of Hysterectomy Route

--

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$48-63,999

1.15

0.80-1.63

1.72

0.91-3.28

1.05

0.65-1.69

1.12

0.73-1.73

$38-47,999

1.07

0.74-1.52

1.53

0.82-2.85

0.89

0.55-1.45

1.13

0.72-1.75

$1-37,999

1.06

0.79-1.43

2.52

1.51-4.21

1.11

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Price 31

0.57

0.38-0.85

--

--

--

--

--

--

--

Medicaid

0.59

0.38-0.90

0.69

0.38-1.25

0.54

0.27-1.08

0.51

0.28-0.94

Medicare

0.96

0.60-1.56

0.90

0.43-1.90

0.73

0.37-1.47

1.35

0.73-2.49

HMO/PPO

1.04

0.82-1.32

0.66

0.44-0.99

1.27

0.93-1.74

1.09

0.79-1.50

SC

Private

--

M AN U

Insurance

0.75-1.64

TE D

MIH, minimally invasive hysterectomy; AOR, adjusted odds ratio; CI, confidence interval; AA, African American; Income Quartile, Median household income quartile; HMO/PPO, health maintenance organization/preferred

EP

provider organization.



AC C

*All minimally invasive hysterectomy includes vaginal, laparoscopic, and robot-assisted hysterectomies AOR adjusted for age, BMI, procedure year, hospital, obstetrical & surgical history, primary diagnosis, uterine

weight, and all other variables reported (race, ethnicity, median household income quartile, insurance status).

Social Determinants of Hysterectomy Route

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Figure 1. Flow diagram of study participants

Social Determinants of Hysterectomy Route

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