Results
A total of 447,479 women ≥18 years old were coded for hysterectomy in
the SID/SASD in Colorado, Florida, Maryland, New Jersey, and New York between 2010
and 2014. After excluding women with an obstetric delivery, complication/history of
delivery, a diagnosis of cancer, a diagnosis of obesity, fibroids, or prior
abdominopelvic surgery, and with missing LOS, the final analytic cohort included
133,082 women ( Supplemental Figure
1 ). Eighty-seven percent (87%) had inpatient surgery (41% vaginal, 25%
laparoscopic, 22% abdominal) and 13% had outpatient surgery (8% laparoscopic, 5%
vaginal, 0.17% abdominal).
Characteristics of the potentially MIS-eligible hysterectomy cohort
stratified by race/ethnicity are summarized in Table
1 . Inpatient surgery was more common for Asians/PIs (91%), AAs (89%), and
Hispanics (88%), compared to White women (87%). AA women were younger at time of
hysterectomy than other groups (median age 44 years for inpatients and 43 years for
outpatients). Sixty-one percent (61%) of AA women had surgery at a high-AA-serving
hospital, followed by Asian/PI women (36%), Hispanic (35%), and White women
(25%).
Abdominal hysterectomy rates decreased 1.7-fold for Whites
( p =0.011 for linear time trend) and 1.6-fold for AAs
( p =0.008) and Hispanics ( p =0.032; Figure 1A ) from 2010 to 2014. Vaginal
hysterectomy rates decreased 1.4-fold for Whites ( p =0.016),
1.5-fold for AAs ( p =0.029), and 1.4-fold for Hispanics
( p =0.041). Laparoscopic hysterectomy rates increased more
slowly during that time for AAs (1.6-fold, p =0.101) than Whites
(1.8-fold, p =0.026) and Hispanics (1.9-fold,
p =0.017; Figure 1C ).
Hysterectomy trends by race/ethnicity from 2010 to 2014 were similar across all five
states (data not shown).
Regardless of payer, AA women underwent more abdominal and fewer vaginal and
laparoscopic hysterectomies than White women ( Supplemental Figure 2 ). Hospitals that
disproportionately served AA women performed more abdominal and fewer vaginal
hysterectomies in all women ( Figure 2 ). All
racial/ethnic groups underwent more abdominal hysterectomies in quintile
5/high-AA-serving hospitals (>16% AA) than in quintile 1/low-AA-serving
hospitals (<2% AA): Whites (23% quintile 5 vs 16% quintile 1), AAs (32%
quintile 5 vs 14% quintile 1), Hispanics (28% quintile 5 vs 17% quintile 1), and
Asians/PIs (32% quintile 5 vs 8% quintile 1). Correspondingly, all groups underwent
fewer vaginal hysterectomies in quintile 5 than in quintile 1. AA (28% quintile 5 vs
41% quintile 1) and Asian/PI women (28% quintile 5 vs 40% quintile 1) underwent
fewer laparoscopic procedures in quintile 5 than in quintile 1.
AA, Hispanic, and Asian/PI women had more abdominal and fewer laparoscopic
procedures than White women across all volume categories ( Figure 3 ). AA and Asian/PI women also had fewer vaginal
procedures than White women did across all volume categories ( Figure 3 ). However, all women had more abdominal and fewer
laparoscopic hysterectomy in low-versus high-volume hospitals, where 38% of
low-volume hospitals performed no laparoscopic hysterectomies ( Supplemental Figure 3 ).
In adjusted analysis, compared to White women, Asian/PI (aPR 0.88, 95% CI
0.81–0.96), AA (aPR 0.93, 95% CI 0.90–0.96), and Hispanic
race/ethnicity (aPR 0.95, 95% CI 0.93–0.97) were associated with decreased
likelihood of vaginal than abdominal hysterectomy ( Figure 4A ). AA (aPR 0.90, 95% CI 0.87–0.94) and Hispanic
race/ethnicity (aPR 0.95, 95% CI 0.92–0.98) were also associated with
decreased likelihood of laparoscopic than abdominal hysterectomy ( Figure 4B ). In a sensitivity analysis including all women
(i.e., regardless of the indication for hysterectomy), AA women had a lower aPR of
receiving vaginal hysterectomy (all women, aPR, 0.90, 95% CI, 0.88–0.92 vs
MIS-eligible, aPR, 0.93, 95% CI, 0.90–0.96) and a lower aPR of receiving
laparoscopic hysterectomy (all women, aPR, 0.85, 95% CI, 0.83–0.87 vs.
MIS-eligible, aPR, 0.90, 95% CI, 0.87–0.94; Supplemental Table 2 ). A similar trend
was seen for Hispanic and Asian/PI women in the laparoscopic model ( Supplemental Table 2 ).
Materials
Hospital discharge data came from the Agency for Healthcare Research and
Quality Healthcare Cost and Utilization Project (HCUP) State Inpatient Databases
(SID) and State Ambulatory Surgery Databases (SASD). The SID are state-specific
databases containing inpatient billing records from acute-care community hospitals
[ 15 ], while the SASD are state-specific
files containing ambulatory surgery billing records from community hospitals [ 15 ]. Data from Colorado, Florida, Maryland, New
Jersey, and New York were used because these states had both SID and SASD files, and
reported race/ethnicity. Florida and New York were selected because their large and
diverse populations allowed the inclusion of more nonwhite women. Because
individuals could not be identified, the study was deemed exempt by the Human
Research Protections Office at Washington University.
Adult women age ≥18 years who underwent hysterectomy for benign
gynecologic conditions between 2010 and 2014 were included ( Supplemental Figure 1 ). Only women who
underwent hysterectomy on day 0/1 of a hospitalization were included from the SID to
avoid procedures due to adverse events. Hysterectomies performed for a complication
of delivery or history of delivery outcome were removed to exclude women undergoing
peripartum hysterectomy. Women coded for uterine, cervical, ovarian,
colon/abdominal, bladder/kidney, or metastatic cancer were excluded to focus on
benign conditions. Women with diagnoses of obesity, fibroids, or history of prior
abdominopelvic surgery were excluded to focus on women likely eligible for MIS.
Encounters with missing length of stay (LOS) were excluded because inpatient versus
outpatient procedures were defined accordingly.
Hysterectomy procedures were classified as abdominal, vaginal, or
laparoscopic (including robotic) using International Classification of
Diseases, Ninth Revision, Clinical Modification (ICD-9-CM) procedure
codes in the SID and Current Procedural Terminology (CPT) codes in the SASD ( Supplemental Table 1 ).
Procedures were classified as inpatient if the LOS was ≥1 day, and outpatient
if the LOS was <1 day. Outpatient procedures in Colorado were identified
using ICD-9-CM procedure codes, due to missing CPT codes in the Colorado SASD.
The exposure variable of interest was race/ethnicity, a 6-level categorical
variable. Race/ethnicity was defined according to HCUP: White, African American
(AA), Hispanic, Asian/Pacific Islander (PI), Native American (NA)/Other, and
missing. Race/ethnicity is collected through patient self-report or hospital staff
observation. Ethnicity takes precedence over race when both are reported by the
state as separate data elements [ 16 ].
Patient-level variables included age, state, year of surgery, payer, and
median household income for zip code as defined by HCUP. The Elixhauser
classification was used for comorbidities [ 17 ]. Benign indications for hysterectomy were categorized using ICD-9-CM
diagnosis codes ( Supplemental
Table 1 ). Abnormal uterine bleeding is a modified grouping based on the
polyp, adenomyosis, leiomyoma, malignancy and hyperplasia, coagulopathy, ovulatory
dysfunction, endometrial, iatrogenic, and not-yet classified (PALM-COEIN)
classification system [ 18 ]. Additional
surgical indications included pelvic pain/endometriosis, ovary-related disorders
(i.e., benign neoplasms, cysts, non-inflammatory disorders of the ovary, and
polycystic ovaries), prolapse, menopause, other female genital organ (FGO) diagnoses
(i.e., benign neoplasms and non-inflammatory disorders of other FGOs), prophylaxis
(i.e., personal/family history of breast/gynecologic cancer), and cervical
dysplasia.
Hospital-level variables, obtained by linking hospital identifiers in the
SID and SASD to the American Hospital Association Annual Survey data, included
hospital location (rural, urban), teaching status (association with a medical
school), and bed-size (small ≤300, medium 300–600, large ≥600).
Annual hospital hysterectomy procedure volume was categorized into low 1–50,
medium 51–200, and high ≥201 based on all hysterectomies performed in
the hospitals for any indication (i.e., benign, malignant, or due to an adverse
event). To determine the association of surgical route for hysterectomy by
race/ethnicity in hospitals that serve a higher versus lower proportion of AA
patients, hospitals were stratified into quintiles based on the proportion of AA
hospitalizations among all hospitalizations at the individual hospitals: quintile 1
(0–2% AA), quintile 2 (2–5% African American), quintile 3 (5–9%
African American), quintile 4 (9–16% African American), and quintile 5
(>16% AA).
We calculated hysterectomy rates/100,000 adult women/year by surgical
approach and race/ethnicity. For each surgical route/procedure and racial/ethnic
group, the hysterectomy rate was computed by dividing the number of women who
underwent hysterectomy in each state in a specific year (numerator) by the number of
women aged ≥18 years at risk (denominator). The data for the numerator were
from the SID and SASD. The data for the denominator were from census data [ 19 ], adjusted for hysterectomy prevalence to
avoid inappropriately retaining women in the population-at-risk denominator who had
a prior hysterectomy [ 20 ]. Annual
hysterectomy prevalence estimates were obtained from the Behavioral Risk Factor
Surveillance System (BRFSS), a nationally representative telephone survey conducted
to collect prevalence data on health measures among U.S. adults [ 21 ]. BRFSS data from adjoining even-numbered years were
used to calculate weighted average prevalence estimates for odd-numbered years. The
corrected population-at-risk denominator
( p c ) was calculated as follows:
p c = p × ( 1 − h ) , where p is the population-at-risk denominator and
h is the hysterectomy prevalence in a specific year [ 20 ].
In unadjusted analyses, linear trends over time for hysterectomy
rates/100,000 adult women/year stratified by surgical route and race/ethnicity were
examined using simple linear regression models with year of surgery as the
independent variable and hysterectomy rate as the dependent variable. The
p -value for time trend was reported, and statistical
significance was determined by p <0.05.
Hysterectomy surgical route was the outcome of interest. We targeted two
outcomes: vaginal versus abdominal hysterectomy (vaginal model) and laparoscopic
versus abdominal hysterectomy (laparoscopic model). In adjusted analyses, we fit a
marginal structural log binomial regression model [ 22 ] to estimate adjusted standardized prevalence ratios (aPRs) for the
(1) race/ethnicity-receipt of vaginal hysterectomy association and (2)
race/ethnicity-receipt of laparoscopic hysterectomy association. This model was
selected over traditional logistic regression because the odds ratio estimated from
logistic regression will only approximate the relative risk when the outcome is rare
[ 22 , 23 ], but in our data, vaginal and laparoscopic hysterectomy were common
outcomes. Use of odds ratios to summarize effects of exposure is discouraged when
outcomes are common due to the concern that odds ratios will be misinterpreted as
relative risks. Our model was also selected over multivariable log-binomial or
log-linear/Poisson models because of convergence and other issues with those models
[ 22 , 23 ]. Confounding was handled by using inverse probability weighting, in
which stabilized weights were used [ 22 ]. For
each woman, the stabilized weight was a ratio of the marginal probability for
one’s own race/ethnicity over the predicted probability for her
race/ethnicity conditional on her individual- and hospital-level characteristics.
For the denominator, we fit a multivariable multinomial logistic model with the 6
racial/ethnic groups as the outcome variable, and covariates including age, state,
year of surgery, payer, income, comorbidities, indications for hysterectomy,
hospital location, hospital bed size, and hysterectomy procedure volume (defined
above). Hospital characteristics were included as covariates because nonwhite women
may seek care at different types of hospitals than White women, and we wanted to
address that variation in our weighting procedure. Using this estimated model, we
predicted the probability for one’s own race/ethnicity based on her level of
each covariate. For the numerator, we fit the same multinomial logistic model
without covariates. Using this estimated model, we predicted the probability for
one’s own race/ethnicity. In the weighted data, all exposure groups under
comparison (i.e., racial/ethnic groups) had a similar distribution of confounding
factors [ 22 ].
We then fit a log binomial model to the weighted data using PROC GENMOD with
binomial distribution and log link function with repeated statement to estimate the
adjusted standardized prevalence ratios [ 22 , 23 ]. The hospital identifier
in the repeated statement was used to account for clustering of hysterectomy
procedures performed within the same hospital. We calculated percentile bootstrap
confidence intervals (CIs) based on 2,000 samples [ 22 ]. We additionally performed a sensitivity analysis for the
race/ethnicity-receipt of vaginal or laparoscopic hysterectomy in all women (i.e.,
including women with fibroids, obesity, or prior abdominopelvic surgery) and
calculated aPRs and percentile bootstrap CIs based on 600 samples. All analyses were
performed with SAS version 9.4 (SAS Institute Inc., Cary, NC).
Conclusion
Among women likely eligible for MIS, AA, Hispanic, and Asian/PI women were
more likely than White women to undergo abdominal hysterectomy. The proportion of
all women undergoing abdominal hysterectomy was highest at hospitals serving higher
proportions of AA persons, and more racial/ethnic minority women sought care at
those hospitals than White women. This difference in treatment type based on site of
care can lead to disparities in outcomes, because of their association with
complications, which is exacerbated by increased length of stay in the hospital.
Evidence of disparities were noticeable in our study and could increase over time if
laparoscopic hysterectomy rates continue to increase more slowly for AA women than
for women of other groups. To better understand what drives hysterectomy treatment
disparities, future studies should examine what distinguishes hospitals providing
lower quality of care as evidenced by higher utilization of abdominal hysterectomy
from those providing higher quality of care with greater utilization of MIS, and
barriers to access to high-volume centers and/or surgical specialists.
Discussion
We compared hysterectomy trends by race/ethnicity over time including
inpatient and ambulatory care data and examined variation in surgical route for
women likely eligible for MIS. Laparoscopic hysterectomy rates in AA women increased
less rapidly over the 5-year time period of our study than in other racial/ethnic
groups. Even after adjusting for confounding factors and controlling for clustering
of procedures within hospitals, compared to White women, we still found that
Asian/PI, AA, and Hispanic women were less likely to receive vaginal hysterectomy,
and AA and Hispanic women were less likely to receive laparoscopic hysterectomy.
By focusing on women likely eligible for MIS we could assess racial/ethnic
disparities more robustly than other recent studies of benign conditions
demonstrating lower use of MIS among nonwhite women [ 1 , 6 , 7 , 9 ]. While our findings do align
with conclusions in previous studies, those studies did not exclude women from
analysis with conditions that could predispose to abdominal hysterectomy and found a
greater strength of association between minority race/ethnicity and receipt of MIS,
ranging from adjusted odds ratios of 0.51–0.70 for AA women [ 1 , 7 , 9 ], 0.24–0.67 for Hispanic women [ 1 , 6 , 9 ], and 0.58 for Asian women [ 1 ] compared to White women. In our sensitivity analysis
that did not exclude women from analysis with conditions that could predispose to
abdominal hysterectomy, the aPRs were further away from 1.00, indicating a greater
difference/disparity in receipt of MIS, particularly for AA women. The wider
observed differences in aPRs for AA women were likely due to their ineligibility for
MIS rather than differences/disparities in treatment. Of note, differences in
treatment for AA women may be wider beyond the end of our study period in 2014 as a
result of the U.S. Food and Drug Administration’s warning in 2014 about the
use of laparoscopic power morcellation during fibroid surgery and the potential for
spread of unsuspected cancer [ 24 ]. This
warning was followed by the banning or restricting of the power morcellator by many
hospitals, and studies have demonstrated a subsequent increase in open hysterectomy
rates following the power morcellation guidelines [ 25 – 27 ]. Because AA women
have more fibroids than other groups [ 12 ],
they are even more likely to receive an open hysterectomy and experience
complications as a result of the warning.
Despite focusing on women likely eligible for MIS, 22% of the women in our
study underwent abdominal hysterectomy. Nonwhite women were more likely than White
women to undergo abdominal hysterectomy, which is associated with more
complications, pain, and longer LOS [ 3 ].
Vaginal hysterectomy is recommended for women with benign conditions, and
laparoscopic hysterectomy is preferred when a vaginal route is infeasible [ 3 ]. Surgeon training and ability to maintain
proficiency in MIS and/or lack of information about alternatives to abdominal
surgery among good candidates for MIS have been cited as explanations for continued
utilization of abdominal hysterectomy [ 28 – 30 ]. We additionally
identified hospital factors that might also contribute to continued utilization of
abdominal hysterectomy and disparities in surgical route. Hospitals serving a higher
proportion of AA persons performed more abdominal and fewer vaginal procedures
across all groups. In addition, lower proportions of AA and Asian/PI women received
laparoscopic procedures in hospitals disproportionately serving AA women compared to
hospitals serving almost exclusively non-AA patients. A higher proportion of
racial/ethnic minority women underwent hysterectomy at high-AA-serving hospitals
than White women, potentially exacerbating disparities in utilization of MIS. We
also found that the proportions of all women undergoing abdominal hysterectomy were
highest at low- and medium-hysterectomy-volume hospitals. Mehta et al. [ 9 ] similarly found that women undergoing
hysterectomy at low-or medium-volume hospitals had higher odds of undergoing
abdominal hysterectomy. Taken together, these findings add to what we know about
racial/ethnic disparities, because 33% of high-hysterectomy-volume hospitals were
also high AA-serving-hospitals, indicating that treatment disparities are not only
correlated with procedural volume but also the type of population served by the
hospital, the latter of which could be a reflection of quality of care [ 31 , 32 ].
High-AA-serving and low-hysterectomy-volume hospitals could lack surgeons with
advanced skills, equipment, staff, or support to perform MIS.
That hospitals primarily serving AA patients performed more open
hysterectomies in all women and more racial/ethnic minority women sought care at
those hospitals is potentially important as an explanation for disparities by
race/ethnicity. It suggests disparities based on site of care and system-level
policy solutions aimed at lowering open hysterectomy and subsequent complication
rates to help all women to maintain quality of life. Solutions might include regular
in-service teachings on emerging hysterectomy techniques, perhaps offering CEU
credits as an incentive, or mentoring for surgeons that perform MIS less frequently.
Loring et al. [ 30 ] demonstrated that a
gynecologic surgery practice could be transformed from primarily abdominal to
primarily laparoscopic via a surgical mentorship program. Partnerships between
hospitals performing fewer MIS and those that perform MIS more frequently might also
provide a mechanism for reducing treatment disparities. Such partnerships could
offer a mechanism to identify women eligible for MIS and referring them to higher
volume hospitals. This is particularly important for women at higher risk for
complications after abdominal hysterectomy. Our findings also suggest the need for
clinical pathways aimed at reducing abdominal hysterectomy in women undergoing
hysterectomy for benign conditions. Sanei-Moghaddam et al. [ 33 ] demonstrated a decrease in the proportion of
abdominal hysterectomy performed after implementation of a clinical hysterectomy
pathway.
Our study has several strengths. We created an all-payer and diverse study
population of women undergoing inpatient and outpatient hysterectomies from five
ethnically/racially diverse states. To reduce bias in associations, we restricted
the population to women likely eligible for MIS to analyze racial/ethnic differences
in surgical route among women who should be candidates for vaginal/laparoscopic
hysterectomy. Prior studies were less representative through their focus on benign
conditions limited to a single institution, hospital system, or state [ 8 , 9 ], one
rather than a range of payers [ 4 ], data
collected by only participating health systems [ 5 ], or inpatient data [ 1 , 7 ]. In contrast to most previous studies [ 1 , 4 – 8 ], we identified
hospital factors that potentially explain continued utilization of abdominal
hysterectomy and treatment disparities (i.e., high-AA-serving hospitals and
procedure volume), allowing us to offer potential solutions to reduce disparities.
Finally, because surgical route varies by indication for surgery [ 3 ], we compared vaginal and laparoscopic hysterectomy to
abdominal hysterectomy separately unlike previous studies [ 1 , 5 , 7 , 9 ].
Our study is not without limitations. Classification of hysterectomy
procedures was based on ICD-9-CM and CPT coding, rendering procedural
misclassification possible. We could not control for uterine size, fibroid tumor
characteristics, body mass index, and patient preference, all of which may influence
if women receive vaginal or laparoscopic surgery [ 3 , 10 ]. Some of the racial/ethnic
differences seen in AA women could be due to residual confounding because obesity is
undercoded in administrative data [ 34 ], and
AA women have higher prevalence of obesity [ 11 ], which can make laparoscopic hysterectomy more difficult [ 10 ]. Additionally, state- and hospital-level
variation exists in how race/ethnicity information is collected by hospitals, which
could lead to inconsistent data [ 35 ].
However, hospital discharge data is reasonably reliable for the focus of our study
[ 36 ]. Finally, we could only identify
comorbidities and evidence of prior abdominopelvic surgery based on the index
hospitalization, adding to misclassification.
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