YGYNO-975525; No. of pages: 6; 4C: Gynecologic Oncology xxx (2014) xxx–xxx
Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
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Haider Mahdi a,⁎, David Lockhart b, Mehdi Moslemi-Kebria a, Peter G. Rose a a
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H I G H L I G H T S
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Gynecologic Oncology division, Ob/Gyn and Women's Health Institute, Cleveland Clinic, Cleveland, OH, USA Department of Biostatistics, University of Washington, Seattle, WA, USA
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• African American patients with endometrial cancer have more preoperative morbidities and less likely to undergo minimally invasive surgery. • African American patients with endometrial cancer are more likely to have postoperative complications including surgical and non-surgical in univariate analysis. • African American race was not an independent predictor of poor 30-day outcomes in multivariable analysis after controlling for other confounders.
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Keywords: Race Surgery Endometrial cancer Morbidity Mortality African American White
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Introduction
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Endometrial cancer is the most common gynecologic malignancy in the United States causing 52,630 incident cases and 8590 deaths in 2014 [1]. Despite the advance in management and significant improvement in survival, disparities in uterine cancer incidence, treatment and outcome between African American and white patients have been increasingly identified over the recent years. African American patients
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Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer
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Objectives. To examine postoperative 30-day morbidity and mortality in African American (AA) compared to white patients (W) with endometrial cancer (EC). Methods. Patients with EC were identified from the American College of Surgeons National Surgical Quality Improvement Program from 2005 to 2011. AA and W subgroups were studied. Multivariable logistic regression models were performed. Results. Of 3248 patients, 2899 (89%) W and 349 (11%) AA were identified. AA were more likely to have diabetes, hypertension, ascites, neurologic morbidities, weight loss, non-independent functional status, higher ASA class, higher serum creatinine ≥2 mg/dl, hypoalbuminemia and anemia. Laparoscopic surgery was performed less frequently in AA than W (41.4% vs. 50.3%, p b 0.001). AA had a significantly higher risk of postoperative complications than W (21% vs. 12%, p b 0.001) including surgical (17% vs. 10%, p b 0.001) and non-surgical complications (7% vs. 4%, p = 0.022). Mean length of hospital stay and operative time were longer in AA than W but there was no difference in surgical re-exploration. In multivariable model after adjustment for confounders including surgical complexity and associated morbidities, AA race was not an independent predictor of “any postoperative complications” for both laparotomy group (OR 1.1, 95% CI 0.73–1.61, p = 0.65) and laparoscopic group (OR 1.43, 95% CI 0.80–2.45, p = 0.21). No difference in 30-day mortality was found between AA and W (1% vs. 1%, p = 0.11). Conclusions. AA patients with EC have more preoperative morbidities, postoperative complications and were less likely to undergo minimally invasive surgery. However, AA race was not an independent predictor of poor 30-day outcomes after controlling for other confounders. © 2014 Published by Elsevier Inc.
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are more likely to present with advanced stage, poorly differentiated and aggressive non-endometrioid cancers compared to white patients [2–5]. Further, African American patients with endometrial cancer are less likely to undergo surgical treatment and have worse survival [4,6–9]. Nonetheless, after controlling for multiple variables including stage, histology, and treatment, African American women with endometrial cancer still have a worse survival than white women [7,3,4]. On the other hand, single institutional data showed no difference in outcome when correcting for other prognostic factors [10]. In the systematic review of the published literature on racial disparities in uterine cancer, Long et al. showed that the increased mortality in African Americans is multifactorial. However, the most consistent contributor
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Article history: Received 25 March 2014 Accepted 24 May 2014 Available online xxxx
⁎ Corresponding author at: Ob/Gyn and Women's Health Institute, 9500 Euclid Ave, Cleveland, OH 44195, USA. Fax: +1 216 445 6325. E-mail address: [email protected] (H. Mahdi).
http://dx.doi.org/10.1016/j.ygyno.2014.05.024 0090-8258/© 2014 Published by Elsevier Inc.
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
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Data source
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ACS NSQIP is a risk-adjusted data collection mechanism that collects and analyzes clinical outcomes data. Participating hospitals use their collected data to develop quality initiatives that improve surgical care and to identify elements in provided health care that can be improved when compared with other institutions. The ACS NSQIP collects data on 135 variables including preoperative risk factors (patient demographics, comorbidities, laboratory values), intraoperative variables, and 30-day postoperative mortality and morbidity outcomes for a systematic and prospective sample of patients undergoing major surgical procedures. Data are collected in a standardized fashion according to strict definitions by dedicated surgical clinical nurse reviewers. Patients are followed throughout their hospital course and after discharge from hospital for up to 30 days postoperatively. A site's Surgical Clinical Reviewer (SCR) captures these data using a variety of methods including medical chart extraction, doctor's office records, 30-day telephone interview with the patients and other methods. Patients who were diagnosed with endometrial cancer were identified from the 2005 to 2011 ACS-NSQIP participant use files, which include data collected from 258 academic and community hospitals throughout the United States using ICD-9 codes. Patients with endometrial cancer were included if they had at least hysterectomy with or without other surgeries using Current Procedural Terminology (CPT) codes. For study purposes, 2 subgroups were abstracted for comparison: White (W) and African American (AA) patients.
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Risk factors and outcome
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All risk factors available in the ACS NSQIP database were compared between the two groups. The primary end points of the study were analysis of 30-day mortality, postoperative morbidity, procedurerelated complications, surgical re-exploration (return to the operating
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Statistical analysis
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Associations between categorical covariates were assessed using Chi-squared test. Group differences in means of continuous measures were assessed using student's t-test or Wilcoxon rank-sum test. The preoperative laboratory values were used both as continuous and categorical variables: serum albumin (N3 versus ≤ 3 mg/dl); hematocrit (b35 versus ≥ 35); serum creatinine (≥2 versus b 2 mg/dl); platelets (b350,000 versus ≥ 350,000 cell/cubic ml); and WBC (b11 versus ≥ 11 cells/cubic ml). The cutoffs for laboratory values were decided based on the percentile (90th or 10th percentile when appropriate) combined with clinically valuable cutoff based on prior literature. To adjust for surgical complexity, patients who underwent additional surgical procedures beside hysterectomy were given a specific score for each procedure. Then, based on the number of procedures performed, the sum of these scores was calculated creating a modified surgical complexity scoring system. A score of 1 was given to any of the following procedures: hysterectomy with or without salpingooophorectomy, lymphadenectomy or omentectomy. A score of 2 was given to any of the following procedures: small or large bowel resection, gastrectomy, hepatectomy, splenectomy and pancreatectomy. Multivariable logistic regression models were used to assess the association between race and 30-day postoperative complications while controlling for all other confounders. For the creation of the models, we considered all preoperative variables available in the ACS NSQIP database, including demographics (age and race), preoperative health status and comorbidities, preoperative laboratory values (serum albumin, creatinine, white cell count, platelet count and hematocrit), and operative factors (operative time, ASA class, surgical complexity). The preoperative morbidities, operative risk factors or demographic variables that were significantly associated with postoperative complications in the univariate logistic regression model with a p value b 0.05 were included in the multivariate regression model. A final logistic regression model was run using the two racial groups and all confounders found in this way. All tests of significance were at the p b 0.05 level, and p values were two-tailed. STATA 10.0 program (College Station, TX) was used for the analysis of the data.
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Results
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3248 patients met the inclusion criteria. Of them, 2899 (89%) were W and 349 (11%) were AA. Demographics and clinical characteristics of each group are shown in Table 1. African American patients with endometrial cancer were more likely to have morbid obesity (p = 0.01), diabetes (p b 0.001), hypertension requiring medications (p b 0.001), ascites (p b 0.001), neurologic morbidities (p = 0.002), weight loss within 6 months prior to surgery (p = 0.01), dependent functional status (p = 0.016), and higher ASA class (p b 0.001). Further, AA were
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Methods
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room within 30 days) and length of hospital stay. The secondary end point was to perform subset analysis looking at laparotomy and laparoscopic approaches. Composite end points were created to categorize postoperative complication into few related groups: surgical complications (all surgical site infections, wound disruption, bleeding requiring transfusion and peripheral nerve injury), renal complications (progressive renal failure, acute renal failure), pulmonary complications (pneumonia, unplanned intubation, respiratory insufficiency requiring ventilation for 48 h), infectious complications (systematic inflammatory response syndrome, sepsis, septic shock, surgical site infection and pneumonia), cardiovascular complications (pulmonary embolism, stroke/cerebrovascular event, cardiac arrest, myocardial infarction, deep vein thrombosis requiring therapy) and any nonsurgical complication (any complication except surgical complications). Patients with pre-operative sepsis were excluded from the study. Patients who are ventilator dependent, with renal failure or on dialysis before surgery were excluded from their respective complication category.
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to incidence and mortality disparities were histology and socioeconomics [11]. Pattern of care studies has shown that African American patients are less likely to undergo surgical treatment when diagnosed with cancer compared to white patients [10,12,13]. African American patients who receive treatment for endometrial cancer are more likely to undergo primary radiotherapy than surgery compared to white women. Furthermore, African American patients who undergo surgery for endometrial cancer are less likely to receive definite surgery than white women [9,4]. Across all tumor types, AA patients who undergo surgery have variable surgical outcomes. African American patients are nine times more likely to experience postoperative mortality following acoustic neuroma resection than white patients [16]. Furthermore, African Americans with breast cancer are 35% more likely to develop postoperative complications and 87% more likely to experience in-hospital mortality than white women [13]. On the other hand, in an analysis of patients undergoing surgical treatment of a variety of thoracic, abdominal and pelvic malignancies, no difference was found in 30-day postoperative complications between white and African American patients [17]. We questioned whether differences in the rates of postoperative morbidity and mortality drive the racial disparity in survival between African American and white patients with endometrial cancer. The information on the differences in short-term postoperative outcomes between these two racial groups are limited. Therefore, the objective of this study is to analyze the difference in the 30-day morbidity and mortality between white and African American women following surgery for endometrial cancer using nationwide data from the American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) database.
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Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
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H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx t1:1 t1:2 Q2
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Table 1 Demographic and clinical characteristics of patients with endometrial cancer stratified by race (n = 3248). Variable
Total cohort
White
African American
t1:4
N
3248
2899
349
t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19 t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26 t1:27 t1:28 t1:29 t1:30 t1:31 t1:32 t1:33 t1:34 t1:35 t1:36 t1:37
Age
1214 1131 615 288
63.2 1080 (37%) 1012 (35%) 550 (19%) 257 (9%) 1096 (38%) 1086 (38%) 700 (24%) 1495 (52%) 1314 (45%) 88 (3%) 55 (2%) 290 (10%) 525 (18%) 1626 (56%) 93 (3%) 39 (3%) 7 (0.2%) 76 (3%) 27 (1%) 38 (1%) 14 (0.5%) 41 (1%) 6 (0.2%) 1457 (50.3%) 8 (0.3%) 2872 (99%) 27 (1%) 319 (11%) 155 (8%) 59 (2%) 163 (6%) 345 (12%)
62.9 134 (38%) 119 (34%) 65 (19%) 31 (9%) 108 (31%) 137 (40%) 99 (29%) 127 (36%) 204 (58%) 18 (5%) 14 (4%) 39 (11%) 89 (26%) 248 (71%) 15 (4%) 7 (2%) 2 (0.1%) 20 (6%) 11 (3%) 11 (3%) 3 (1%) 1 (0.3%) 1 (0.3%) 455 (41.4%) 2 (1%) 347 (99%) 2 (1%) 94 (27%) 34 (15%) 21 (6%) 21 (6%) 76 (23%)
Functional status Current smoker (within 1 year) Diabetes Hypertension on medications Cardiac comorbidities Respiratory comorbidities Renal comorbidities Neurologic comorbidities Ascites 10% weight loss within 6 months prior to surgery Blood transfusion prior to surgery Steroid use Chemotherapy prior to surgery Surgical approach Emergency Surgical complexity
Laparoscopy
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0–3 N3
C
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Pre-operative anemia (hematocrit b35) Preoperative hypoalbuminemia (serum albumin ≤ 3 g/dl) Preoperative high serum creatinine ≥ 2 Preoperative leukocytosis (N11) Preoperative thrombocytosis (≥350,000 cell/cubic ml)
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Postoperative complications
200
The rates and differences in risk of postoperative complications between AA and W patients stratified by surgical approach are listed in Table 2. AA patients had a significantly higher risk of any postoperative complication than W patients (21% vs. 12%, p b 0.001, Table 2). Further, AA had a higher mean number of postoperative complications compared to W patients (mean 22 in 1000 vs. 15 in 1000, p = 0.007). AA patients had a higher rate of surgical (17% vs. 10%, p b 0.001) and nonsurgical complications (7% vs. 4%, p = 0.022) compared to W patients
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more likely to have higher serum creatinine ≥2 mg/dl (p b 0.001), hypoalbuminemia (serum albumin ≤ 3 mg/dl) (p b 0.001) and anemia (hematocrit b35 mg/dl) (p b 0.001) (Table 1). Laparoscopic surgery was performed less frequently in AA patients than W patients (41.4% vs. 50.3%, p b 0.001, Fig. 1).
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1622 1518 106 69 329 614 1874 108 102 9 96 38 49 17 42 7 1912 10 3219 29 413 189 80 184 421
Fig. 1. Distribution of surgical approach in African American and white patients who underwent surgery for endometrial cancer (p b 0.001).
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ASA class
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BMI
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Mean b60 60–69 70–79 ≥80 0–29 30–39 ≥40 1–2 3 ≥4 Dependent
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t1:3
p-Value
0.62 0.97
0.038
b0.001
0.009 0.49 b0.001 b0.001 0.28 0.19 0.26 0.001 b0.001 0.008 0.35 0.08 0.20 b0.001 0.34 0.50 b0.001 b0.001 b0.001 0.79 b0.001
(Table 2). Among non-surgical complications, infectious (9% vs. 6%, p = 0.009) and pulmonary (3% vs. 1%, p = 0.014) complications were significantly higher among AA than W patients (Table 2). However, there was no significant difference in rate of cardiac (1% vs. 2%, p = 0.30) or renal complications (1% vs. 0.4%, p = 0.23) between AA and W patients. Among the laparotomy group, the rate of any postoperative complication (28% vs. 19%, p = 0.001), surgical (23% vs. 16%, p = 0.016) and non-surgical (10% vs. 6%, p = 0.029) was significantly higher among AA compared to W patients. Among non-surgical complications, pulmonary (5% vs. 2%, p = 0.007) was significantly higher among AA compared to W patients. However, there was no significant difference in rate of cardiac (2% vs. 3%, p = 0.42), infectious (12% vs. 9%, p = 0.12) or renal (2% vs. 1%, p = 0.46) complications between AA and W patients (Table 2). In contrast, among patients who underwent laparoscopic surgery for endometrial cancer, there was no difference in the rate of surgical (3% vs. 3%, p = 0.78), non-surgical (1% vs. 3%, p = 0.47) including pulmonary (0% vs. 1%, p = 0.62), cardiac (0% vs. 1%, p = 0.27), renal (0% vs. 0.1%, p = 0.78) or infectious (3% vs. 3%, p = 0.86) complications between AA and W patients (Table 2). No difference in surgical re-exploration was found between AA and W patients among the entire cohort (1% vs. 2%, p = 0.48), laparotomy group (2% vs. 2%, p = 0.45) and laparoscopy group (0% vs. 1%, p = 0.49). Mean length of hospital stay (4.2 days vs. 3.1 days, p = 0.035) and operative time (185.3 min vs. 173.4 min, p = 0.007) were significantly longer in AA compared to W patients. Among the surgical and non-surgical complications, AA patients had significantly higher risk of intra-operative bleeding requiring blood transfusion of N4 units of packed red blood cells (10% vs. 5%, p b 0.001), pneumonia (2% vs. 1%, p = 0.002), sepsis (3% vs. 1%, p = 0.04). But no difference was found in the risk of surgical site infection (6% vs. 5%, p = 0.15), wound disruption (1% vs. 1%, p = 0.89),
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
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Table 2 Operative parameters and 30-day outcomes among patients who underwent surgery for endometrial cancer stratified by race.
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Pulmonary complications
Cardiac complications
Infectious complications
Any complication
Surgical re-exploration
Mean length of hospital stay (days)
Mean no. of complications
Mean operative time (min)
Operative time
66 (2%) 781 (24%) 1046 (35%) 1355 (42%)
t3:1 t3:2 t3:3
Table 3 Multivariate regression analysis for “any complication” within 30 days following laparotomy for endometrial cancer.
O
R
R
242
unplanned intubation (1% vs. 1%, p = 0.66), respiratory insufficiency requiring ventilation for 48 h (0.3% vs. 0.4%, p = 0.78), septic shock (0.3% vs. 1%, p = 0.27), cardiac arrest (0.3% vs. 0.2%, p = 0.76),
Variable
t3:5 t3:6 t3:7 t3:8 t3:9 t3:10 t3:11 t3:12 t3:13 t3:14 t3:15 t3:16 t3:17 t3:18 t3:19 t3:20 t3:21 t3:22 t3:23 t3:24 t3:25 t3:26
African American BMI 30–39 BMI ≥ 40 Surgical complexity N3 Diabetes Respiratory comorbidities Cardiac comorbidities Hypertension Ascites Neurologic comorbidities 10% weight loss within 6 months prior to surgery Preoperative blood transfusion ASA class 3 ASA class 4–5 Operative time 1–2 h Operative time 2–3 h Operative time N3 h Serum creatinine ≥2 Albumin ≥4 Anemia (hematocrit ≥35) High WBC count (N11,000) Platelets count ≥350,000 cell/cubic ml
U
N
C
t3:4
Open OR (95% CI)
p-Value
1.1 (0.73–1.61) 0.85 (0.59–1.22) 1.35 (0.92–1.97) 4.1 (1.38–12.45) 1.1 (0.76–1.52) 1.46 (0.72–2.81) 1.71 (0.9–3.1) 1.03 (0.74–1.44) 3.86 (1.53–9.6) 1.92 (1.01–3.54) 3.43 (1.44–8.16) 4.05 (0.94–21.12) 1.27 (0.91–1.78) 2.57 (1.31–4.95) 0.8 (0.32–2.33) 0.98 (0.4–2.84) 1.6 (0.66–4.64) 1.41 (0.71–2.71) 0.70 (0.44–1.14) 0.45 (1.39–3.53) 2.23 (0.7–1.53) 1.04 (0.7–1.53)
0.65 0.37 0.12 0.01 0.65 0.26 0.08 0.86 0.003 0.04 0.005 0.069 0.16 0.005 0.64 0.96 0.33 0.38 0.14 0.007 0.83 0.83
19 (0.7%) 15 (1%) 4 (0.3%) 282 (10%) 234 (16%) 48 (3%) 118 (4%) 81 (6%) 37 (3%) 14 (0.5%) 13 (1%) 1 (0.7%) 38 (1%) 24 (2%) 14 (1%) 56 (2%) 40 (3%) 16 (1%) 167 (6%) 130 (9%) 37 (3%) 348 (12%) 275 (19%) 73 (5%) 53 (2%) 35 (2%) 18 (1%) 3.2 4.8 1.5 0.15 0.24 0.05 174
5 (1.5%) 5 (2%) 0 (0%) 58 (17%) 55 (23%) 3 (3%) 24 (7%) 23 (10%) 1 (1%) 9 (1%) 4 (2%) 0 (0%) 11 (3%) 11 (5%) 0 (0%) 4 (1%) 4 (2%) 0 (0%) 33 (9%) 30 (12%) 3 (3%) 72 (21%) 68 (28%) 4 (4%) 4 (1%) 4 (2%) 0 (0%) 4.3 5.3 2.0 0.22 0.31 0.04 186
0.11 0.18 0.59 b0.001 0.01 0.78 0.01 0.02 0.29 0.11 0.27 0.78 0.007 0.003 0.30 0.30 0.31 0.27 0.006 0.09 0.86 b0.001 0.001 0.55 0.35 0.45 0.24 0.03 0.61 0.001 0.007 0.13 0.47 0.007
6 (2%) 73 (21%) 106 (30%) 164 (47%)
0.18
F
Renal complications
p-Value
O
Non-surgical complications
African American n (%)
R O
Surgical complications
24 (0.8%) 20 (1.2%) 4 (0.3%) 340 (12.5%) 289 (17%) 51 (3%) 142 (4.4%) 104 (6%) 38 (2.4%) 18 (0.5%) 17 (1%) 1 (0.06%) 49 (1.5%) 35 (2%) 14 (0.9%) 60 (1.8%) 44 (2.6%) 16 (1%) 200 (6.2%) 160 (9.5%) 40 (2.6%) 420 (13%) 343 (20%) 77 (5%) 57 (1.8%) 39 (2%) 18 (1%)
White n (%)
P
Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy ≤60 min 61–120 min 121–180 min ≥180 min
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Mortality
E
t2:4 t2:5 t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23 t2:24 t2:25 t2:26 t2:27 t2:28 t2:29 t2:30 t2:31 t2:32 t2:33 t2:34 t2:35 t2:36 t2:37 t2:38 t2:39 t2:40 t2:41 t2:42 t2:43
Total cohort
T
Variable
60 (2%) 708 (24%) 940 (32%) 1191 (41%)
C
t2:3
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t2:1 t2:2
H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx
myocardial infarction (0% vs. 0.2%, p = 0.99) and peripheral nerve injury (0% vs. 0.1%). In multivariable logistic regression model after adjustment for all confounders including surgical complexity and associated morbidities, AA race was not an independent predictor of “any postoperative complications” for both laparotomy group (OR 1.1, 95% CI 0.73–1.61, p = 0.65, Table 3) and laparoscopic group (OR 1.43, 95% CI 0.80–2.45, p = 0.21, Table 4).
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30-day postoperative mortality
251
No difference in 30-day mortality was found between AA and W patients for the entire cohort (1% vs. 1%, p = 0.11), laparoscopic group (0% vs. 0.3%, p = 0.59) and laparotomy group (2% vs. 1%, p = 0.18, Table 2). In multivariable logistic regression model, AA race was not
252 253
Table 4 Multivariate regression analysis for “any complication” within 30 days following laparoscopic surgery for endometrial cancer.
245 246 247 248 249 250
254 255 t4:1 t4:2 t4:3
Variable
OR (95% CI)
p-Value
t4:4
African American Cardiac comorbidities Hypertension ASA class 3 ASA class 4–5 Albumin ≥4 Anemia (hematocrit ≥35) High WBC count (N11,000)
0.55 (0.16–1.39) 2.03 (0.58–5.48) 0.1.36 (0.82–2.30) 1.29 (0.78–2.14) 2.02 (0.45–6.41) 2.49 (0.50–4.55) 0.35 (0.20–0.67) 1.57 (0.53–3.76)
0.26 0.20 0.24 0.32 0.28 0.38 0.0008 0.35
t4:5 t4:6 t4:7 t4:8 t4:9 t4:10 t4:11 t4:12
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx
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Conflict of interest
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All authors declare no conflict of interest. Funding
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No funding source.
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In this study using the ACS-NSQIP database, we found that African American patients with endometrial cancer were more likely to have higher levels of preoperative morbidities, and less likely to have minimally invasive surgery. African American patients had higher rates of postoperative complications following surgical staging for endometrial cancer compared to their white counterpart. Both surgical and nonsurgical complications were significantly higher in African American patients. Among non-surgical complications, only infectious and pulmonary complications were significantly higher among African American compared to white patients, while no significant difference was found in the rate of cardiac and renal complications between the two racial groups. On the other hand, in multivariate analysis after adjusting for pre-operative morbidities and surgical complexity, African American race was not an independent predictor of adverse 30-day postoperative outcome following surgery for endometrial cancer. As one of the largest multihospital studies to examine risks for developing adverse operative outcomes after cancer surgery across the two racial groups, our results suggest that the 30-day postoperative outcome after endometrial cancer surgery in African American women is comparable to their white counterpart when controlling for preoperative morbidities and surgical complexity. Prior reports on racial disparities of short-term postoperative outcomes in endometrial cancer are limited. Parsons et al. reported no difference in the rate of 30-day postoperative outcomes in racial minority patients undergoing cancer at ACS-NSQIP hospitals compared to white patients [17]. In this study, African American patients were more likely to have pre-operative morbidities compared to white patients. Some of these pre-operative morbidities were significantly associated with adverse postoperative outcome in multivariate analysis like ascites, preoperative weight loss (10% within 6 months), neurologic comorbidities and anemia. These findings might explain at least partially the observed difference in short term postoperative outcome between the two racial groups. Therefore, it is important to focus on managing these morbidities prior to surgery in order to minimize postoperative complications. Minimally invasive surgery has been recently introduced in managing endometrial cancer patients. It is well established that minimally invasive surgery is associated with less peri-operative complications, shorter hospital stay and faster recovery [18,19]. Interestingly, African American patients were less likely to undergo minimally invasive surgery compared to their white counterpart. This could be related to higher frequency of pre-operative comorbidities in African American patients and possibly other socio-economic factors. On the other hand, no difference in surgical complexity was found between the two racial groups. Therefore, increasing the likelihood of minimally invasive approach might help decrease the risk of postoperative complications in this patient population. In this study, other independent predictors of adverse postoperative morbidity after laparotomy for endometrial cancer included surgical complexity, neurologic comorbidities, ascites, pre-operative weight loss (10% within 6 months), anemia, leukocytosis and higher ASA class. Previous studies have identified risk factors for post-operative complications following surgical treatment of endometrial cancer, including older age, obesity (BMI ≥50), preoperative WBC count, higher ASA class, laparotomy and surgical complexity [19,20]. Additionally, renal insufficiency (preoperative creatinine N 1.5 mg/dL) and hypoalbuminemia are associated with more postoperative complications and are independent risk factors of postoperative complications following surgical treatment of gynecologic malignancies [20,21]. Therefore, the higher rate of postoperative complications noticed in univariate analysis in African American women with endometrial cancer could be attributed to the greater number of preoperative comorbidities in these patients.
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Discussion
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Although our study provides insight into the short-term operative outcomes across the two racial groups in ACS NSQIP, we acknowledge several limitations. First, we lacked information on patients' socioeconomic and insurance status, which have been shown to correlate with race. Alternatively, it is also possible that African American patients treated within ACS NSQIP hospitals are carriers of a more favorable health care coverage when compared with other patients who typically cluster at lower-quality hospitals. Second, we did not adjust for surgeon or hospital volume, which has been associated with surgical outcomes. Third, our results were not adjusted for stage at cancer diagnosis, which typically impacts use of effective cancer care and overall survival outcomes. However, we adjusted for extent of surgical treatment, which can act as a proxy for extent of cancer. Despite these limitations, we present evidence of relatively comparable short-term operative outcomes across the two racial groups from more than 250 qualityseeking hospitals that go beyond mortality to examine other important short-term operative outcomes. Ultimately, African American race was not independently associated with a greater risk for postoperative complications or mortality following endometrial cancer surgery. The propensity for African American patients to experience complications is only seen on univariate analysis and likely reflects their preoperative comorbidities as well as the likelihood that they undergo an open staging procedure. Therefore, more efforts should be directed to optimally manage the preoperative comorbidities in this patient population in order to achieve postoperative outcome equivalent to their white counterpart. Further, increasing the likelihood of performing minimally invasive surgery in African American patients with endometrial cancer should be considered if appropriate to decrease the rate of postoperative complications. Further research should be directed to identify the factors contributing to having higher rates of pre-operative comorbidities and lower likelihood of minimally invasive surgery in African American patients with endometrial cancer.
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an independent predictor of 30-day postoperative mortality for the entire cohort (OR 1.4, 95% CI 0.46–3.8, p = 0.48).
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[14,15]
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Contents lists available at ScienceDirect
Gynecologic Oncology journal homepage: www.elsevier.com/locate/ygyno
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Haider Mahdi a,⁎, David Lockhart b, Mehdi Moslemi-Kebria a, Peter G. Rose a a
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Gynecologic Oncology division, Ob/Gyn and Women's Health Institute, Cleveland Clinic, Cleveland, OH, USA Department of Biostatistics, University of Washington, Seattle, WA, USA
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• African American patients with endometrial cancer have more preoperative morbidities and less likely to undergo minimally invasive surgery. • African American patients with endometrial cancer are more likely to have postoperative complications including surgical and non-surgical in univariate analysis. • African American race was not an independent predictor of poor 30-day outcomes in multivariable analysis after controlling for other confounders.
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Keywords: Race Surgery Endometrial cancer Morbidity Mortality African American White
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Introduction
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Endometrial cancer is the most common gynecologic malignancy in the United States causing 52,630 incident cases and 8590 deaths in 2014 [1]. Despite the advance in management and significant improvement in survival, disparities in uterine cancer incidence, treatment and outcome between African American and white patients have been increasingly identified over the recent years. African American patients
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Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer
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Objectives. To examine postoperative 30-day morbidity and mortality in African American (AA) compared to white patients (W) with endometrial cancer (EC). Methods. Patients with EC were identified from the American College of Surgeons National Surgical Quality Improvement Program from 2005 to 2011. AA and W subgroups were studied. Multivariable logistic regression models were performed. Results. Of 3248 patients, 2899 (89%) W and 349 (11%) AA were identified. AA were more likely to have diabetes, hypertension, ascites, neurologic morbidities, weight loss, non-independent functional status, higher ASA class, higher serum creatinine ≥2 mg/dl, hypoalbuminemia and anemia. Laparoscopic surgery was performed less frequently in AA than W (41.4% vs. 50.3%, p b 0.001). AA had a significantly higher risk of postoperative complications than W (21% vs. 12%, p b 0.001) including surgical (17% vs. 10%, p b 0.001) and non-surgical complications (7% vs. 4%, p = 0.022). Mean length of hospital stay and operative time were longer in AA than W but there was no difference in surgical re-exploration. In multivariable model after adjustment for confounders including surgical complexity and associated morbidities, AA race was not an independent predictor of “any postoperative complications” for both laparotomy group (OR 1.1, 95% CI 0.73–1.61, p = 0.65) and laparoscopic group (OR 1.43, 95% CI 0.80–2.45, p = 0.21). No difference in 30-day mortality was found between AA and W (1% vs. 1%, p = 0.11). Conclusions. AA patients with EC have more preoperative morbidities, postoperative complications and were less likely to undergo minimally invasive surgery. However, AA race was not an independent predictor of poor 30-day outcomes after controlling for other confounders. © 2014 Published by Elsevier Inc.
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are more likely to present with advanced stage, poorly differentiated and aggressive non-endometrioid cancers compared to white patients [2–5]. Further, African American patients with endometrial cancer are less likely to undergo surgical treatment and have worse survival [4,6–9]. Nonetheless, after controlling for multiple variables including stage, histology, and treatment, African American women with endometrial cancer still have a worse survival than white women [7,3,4]. On the other hand, single institutional data showed no difference in outcome when correcting for other prognostic factors [10]. In the systematic review of the published literature on racial disparities in uterine cancer, Long et al. showed that the increased mortality in African Americans is multifactorial. However, the most consistent contributor
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Article history: Received 25 March 2014 Accepted 24 May 2014 Available online xxxx
⁎ Corresponding author at: Ob/Gyn and Women's Health Institute, 9500 Euclid Ave, Cleveland, OH 44195, USA. Fax: +1 216 445 6325. E-mail address: [email protected] (H. Mahdi).
http://dx.doi.org/10.1016/j.ygyno.2014.05.024 0090-8258/© 2014 Published by Elsevier Inc.
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
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Data source
102 103
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ACS NSQIP is a risk-adjusted data collection mechanism that collects and analyzes clinical outcomes data. Participating hospitals use their collected data to develop quality initiatives that improve surgical care and to identify elements in provided health care that can be improved when compared with other institutions. The ACS NSQIP collects data on 135 variables including preoperative risk factors (patient demographics, comorbidities, laboratory values), intraoperative variables, and 30-day postoperative mortality and morbidity outcomes for a systematic and prospective sample of patients undergoing major surgical procedures. Data are collected in a standardized fashion according to strict definitions by dedicated surgical clinical nurse reviewers. Patients are followed throughout their hospital course and after discharge from hospital for up to 30 days postoperatively. A site's Surgical Clinical Reviewer (SCR) captures these data using a variety of methods including medical chart extraction, doctor's office records, 30-day telephone interview with the patients and other methods. Patients who were diagnosed with endometrial cancer were identified from the 2005 to 2011 ACS-NSQIP participant use files, which include data collected from 258 academic and community hospitals throughout the United States using ICD-9 codes. Patients with endometrial cancer were included if they had at least hysterectomy with or without other surgeries using Current Procedural Terminology (CPT) codes. For study purposes, 2 subgroups were abstracted for comparison: White (W) and African American (AA) patients.
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Risk factors and outcome
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All risk factors available in the ACS NSQIP database were compared between the two groups. The primary end points of the study were analysis of 30-day mortality, postoperative morbidity, procedurerelated complications, surgical re-exploration (return to the operating
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104 105 106 107 108 109 110 111 112 113 114 115 116 117 118 119 120 121 122 123 124
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Statistical analysis
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134 135 136 137 138 139 140 141 142 143 144 145 146 147 148
Associations between categorical covariates were assessed using Chi-squared test. Group differences in means of continuous measures were assessed using student's t-test or Wilcoxon rank-sum test. The preoperative laboratory values were used both as continuous and categorical variables: serum albumin (N3 versus ≤ 3 mg/dl); hematocrit (b35 versus ≥ 35); serum creatinine (≥2 versus b 2 mg/dl); platelets (b350,000 versus ≥ 350,000 cell/cubic ml); and WBC (b11 versus ≥ 11 cells/cubic ml). The cutoffs for laboratory values were decided based on the percentile (90th or 10th percentile when appropriate) combined with clinically valuable cutoff based on prior literature. To adjust for surgical complexity, patients who underwent additional surgical procedures beside hysterectomy were given a specific score for each procedure. Then, based on the number of procedures performed, the sum of these scores was calculated creating a modified surgical complexity scoring system. A score of 1 was given to any of the following procedures: hysterectomy with or without salpingooophorectomy, lymphadenectomy or omentectomy. A score of 2 was given to any of the following procedures: small or large bowel resection, gastrectomy, hepatectomy, splenectomy and pancreatectomy. Multivariable logistic regression models were used to assess the association between race and 30-day postoperative complications while controlling for all other confounders. For the creation of the models, we considered all preoperative variables available in the ACS NSQIP database, including demographics (age and race), preoperative health status and comorbidities, preoperative laboratory values (serum albumin, creatinine, white cell count, platelet count and hematocrit), and operative factors (operative time, ASA class, surgical complexity). The preoperative morbidities, operative risk factors or demographic variables that were significantly associated with postoperative complications in the univariate logistic regression model with a p value b 0.05 were included in the multivariate regression model. A final logistic regression model was run using the two racial groups and all confounders found in this way. All tests of significance were at the p b 0.05 level, and p values were two-tailed. STATA 10.0 program (College Station, TX) was used for the analysis of the data.
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Results
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3248 patients met the inclusion criteria. Of them, 2899 (89%) were W and 349 (11%) were AA. Demographics and clinical characteristics of each group are shown in Table 1. African American patients with endometrial cancer were more likely to have morbid obesity (p = 0.01), diabetes (p b 0.001), hypertension requiring medications (p b 0.001), ascites (p b 0.001), neurologic morbidities (p = 0.002), weight loss within 6 months prior to surgery (p = 0.01), dependent functional status (p = 0.016), and higher ASA class (p b 0.001). Further, AA were
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room within 30 days) and length of hospital stay. The secondary end point was to perform subset analysis looking at laparotomy and laparoscopic approaches. Composite end points were created to categorize postoperative complication into few related groups: surgical complications (all surgical site infections, wound disruption, bleeding requiring transfusion and peripheral nerve injury), renal complications (progressive renal failure, acute renal failure), pulmonary complications (pneumonia, unplanned intubation, respiratory insufficiency requiring ventilation for 48 h), infectious complications (systematic inflammatory response syndrome, sepsis, septic shock, surgical site infection and pneumonia), cardiovascular complications (pulmonary embolism, stroke/cerebrovascular event, cardiac arrest, myocardial infarction, deep vein thrombosis requiring therapy) and any nonsurgical complication (any complication except surgical complications). Patients with pre-operative sepsis were excluded from the study. Patients who are ventilator dependent, with renal failure or on dialysis before surgery were excluded from their respective complication category.
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to incidence and mortality disparities were histology and socioeconomics [11]. Pattern of care studies has shown that African American patients are less likely to undergo surgical treatment when diagnosed with cancer compared to white patients [10,12,13]. African American patients who receive treatment for endometrial cancer are more likely to undergo primary radiotherapy than surgery compared to white women. Furthermore, African American patients who undergo surgery for endometrial cancer are less likely to receive definite surgery than white women [9,4]. Across all tumor types, AA patients who undergo surgery have variable surgical outcomes. African American patients are nine times more likely to experience postoperative mortality following acoustic neuroma resection than white patients [16]. Furthermore, African Americans with breast cancer are 35% more likely to develop postoperative complications and 87% more likely to experience in-hospital mortality than white women [13]. On the other hand, in an analysis of patients undergoing surgical treatment of a variety of thoracic, abdominal and pelvic malignancies, no difference was found in 30-day postoperative complications between white and African American patients [17]. We questioned whether differences in the rates of postoperative morbidity and mortality drive the racial disparity in survival between African American and white patients with endometrial cancer. The information on the differences in short-term postoperative outcomes between these two racial groups are limited. Therefore, the objective of this study is to analyze the difference in the 30-day morbidity and mortality between white and African American women following surgery for endometrial cancer using nationwide data from the American College of Surgeons (ACS) National Surgical Quality Improvement Program (NSQIP) database.
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Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
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H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx t1:1 t1:2 Q2
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Table 1 Demographic and clinical characteristics of patients with endometrial cancer stratified by race (n = 3248). Variable
Total cohort
White
African American
t1:4
N
3248
2899
349
t1:5 t1:6 t1:7 t1:8 t1:9 t1:10 t1:11 t1:12 t1:13 t1:14 t1:15 t1:16 t1:17 t1:18 t1:19 t1:20 t1:21 t1:22 t1:23 t1:24 t1:25 t1:26 t1:27 t1:28 t1:29 t1:30 t1:31 t1:32 t1:33 t1:34 t1:35 t1:36 t1:37
Age
1214 1131 615 288
63.2 1080 (37%) 1012 (35%) 550 (19%) 257 (9%) 1096 (38%) 1086 (38%) 700 (24%) 1495 (52%) 1314 (45%) 88 (3%) 55 (2%) 290 (10%) 525 (18%) 1626 (56%) 93 (3%) 39 (3%) 7 (0.2%) 76 (3%) 27 (1%) 38 (1%) 14 (0.5%) 41 (1%) 6 (0.2%) 1457 (50.3%) 8 (0.3%) 2872 (99%) 27 (1%) 319 (11%) 155 (8%) 59 (2%) 163 (6%) 345 (12%)
62.9 134 (38%) 119 (34%) 65 (19%) 31 (9%) 108 (31%) 137 (40%) 99 (29%) 127 (36%) 204 (58%) 18 (5%) 14 (4%) 39 (11%) 89 (26%) 248 (71%) 15 (4%) 7 (2%) 2 (0.1%) 20 (6%) 11 (3%) 11 (3%) 3 (1%) 1 (0.3%) 1 (0.3%) 455 (41.4%) 2 (1%) 347 (99%) 2 (1%) 94 (27%) 34 (15%) 21 (6%) 21 (6%) 76 (23%)
Functional status Current smoker (within 1 year) Diabetes Hypertension on medications Cardiac comorbidities Respiratory comorbidities Renal comorbidities Neurologic comorbidities Ascites 10% weight loss within 6 months prior to surgery Blood transfusion prior to surgery Steroid use Chemotherapy prior to surgery Surgical approach Emergency Surgical complexity
Laparoscopy
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Pre-operative anemia (hematocrit b35) Preoperative hypoalbuminemia (serum albumin ≤ 3 g/dl) Preoperative high serum creatinine ≥ 2 Preoperative leukocytosis (N11) Preoperative thrombocytosis (≥350,000 cell/cubic ml)
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Postoperative complications
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The rates and differences in risk of postoperative complications between AA and W patients stratified by surgical approach are listed in Table 2. AA patients had a significantly higher risk of any postoperative complication than W patients (21% vs. 12%, p b 0.001, Table 2). Further, AA had a higher mean number of postoperative complications compared to W patients (mean 22 in 1000 vs. 15 in 1000, p = 0.007). AA patients had a higher rate of surgical (17% vs. 10%, p b 0.001) and nonsurgical complications (7% vs. 4%, p = 0.022) compared to W patients
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more likely to have higher serum creatinine ≥2 mg/dl (p b 0.001), hypoalbuminemia (serum albumin ≤ 3 mg/dl) (p b 0.001) and anemia (hematocrit b35 mg/dl) (p b 0.001) (Table 1). Laparoscopic surgery was performed less frequently in AA patients than W patients (41.4% vs. 50.3%, p b 0.001, Fig. 1).
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1622 1518 106 69 329 614 1874 108 102 9 96 38 49 17 42 7 1912 10 3219 29 413 189 80 184 421
Fig. 1. Distribution of surgical approach in African American and white patients who underwent surgery for endometrial cancer (p b 0.001).
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p-Value
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b0.001
0.009 0.49 b0.001 b0.001 0.28 0.19 0.26 0.001 b0.001 0.008 0.35 0.08 0.20 b0.001 0.34 0.50 b0.001 b0.001 b0.001 0.79 b0.001
(Table 2). Among non-surgical complications, infectious (9% vs. 6%, p = 0.009) and pulmonary (3% vs. 1%, p = 0.014) complications were significantly higher among AA than W patients (Table 2). However, there was no significant difference in rate of cardiac (1% vs. 2%, p = 0.30) or renal complications (1% vs. 0.4%, p = 0.23) between AA and W patients. Among the laparotomy group, the rate of any postoperative complication (28% vs. 19%, p = 0.001), surgical (23% vs. 16%, p = 0.016) and non-surgical (10% vs. 6%, p = 0.029) was significantly higher among AA compared to W patients. Among non-surgical complications, pulmonary (5% vs. 2%, p = 0.007) was significantly higher among AA compared to W patients. However, there was no significant difference in rate of cardiac (2% vs. 3%, p = 0.42), infectious (12% vs. 9%, p = 0.12) or renal (2% vs. 1%, p = 0.46) complications between AA and W patients (Table 2). In contrast, among patients who underwent laparoscopic surgery for endometrial cancer, there was no difference in the rate of surgical (3% vs. 3%, p = 0.78), non-surgical (1% vs. 3%, p = 0.47) including pulmonary (0% vs. 1%, p = 0.62), cardiac (0% vs. 1%, p = 0.27), renal (0% vs. 0.1%, p = 0.78) or infectious (3% vs. 3%, p = 0.86) complications between AA and W patients (Table 2). No difference in surgical re-exploration was found between AA and W patients among the entire cohort (1% vs. 2%, p = 0.48), laparotomy group (2% vs. 2%, p = 0.45) and laparoscopy group (0% vs. 1%, p = 0.49). Mean length of hospital stay (4.2 days vs. 3.1 days, p = 0.035) and operative time (185.3 min vs. 173.4 min, p = 0.007) were significantly longer in AA compared to W patients. Among the surgical and non-surgical complications, AA patients had significantly higher risk of intra-operative bleeding requiring blood transfusion of N4 units of packed red blood cells (10% vs. 5%, p b 0.001), pneumonia (2% vs. 1%, p = 0.002), sepsis (3% vs. 1%, p = 0.04). But no difference was found in the risk of surgical site infection (6% vs. 5%, p = 0.15), wound disruption (1% vs. 1%, p = 0.89),
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
208 209 210 211 212 213 214 215 216 217 218 219 220 221 222 223 224 225 226 227 228 229 230 231 232 233 234 235 236 237 238 239
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Table 2 Operative parameters and 30-day outcomes among patients who underwent surgery for endometrial cancer stratified by race.
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Pulmonary complications
Cardiac complications
Infectious complications
Any complication
Surgical re-exploration
Mean length of hospital stay (days)
Mean no. of complications
Mean operative time (min)
Operative time
66 (2%) 781 (24%) 1046 (35%) 1355 (42%)
t3:1 t3:2 t3:3
Table 3 Multivariate regression analysis for “any complication” within 30 days following laparotomy for endometrial cancer.
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unplanned intubation (1% vs. 1%, p = 0.66), respiratory insufficiency requiring ventilation for 48 h (0.3% vs. 0.4%, p = 0.78), septic shock (0.3% vs. 1%, p = 0.27), cardiac arrest (0.3% vs. 0.2%, p = 0.76),
Variable
t3:5 t3:6 t3:7 t3:8 t3:9 t3:10 t3:11 t3:12 t3:13 t3:14 t3:15 t3:16 t3:17 t3:18 t3:19 t3:20 t3:21 t3:22 t3:23 t3:24 t3:25 t3:26
African American BMI 30–39 BMI ≥ 40 Surgical complexity N3 Diabetes Respiratory comorbidities Cardiac comorbidities Hypertension Ascites Neurologic comorbidities 10% weight loss within 6 months prior to surgery Preoperative blood transfusion ASA class 3 ASA class 4–5 Operative time 1–2 h Operative time 2–3 h Operative time N3 h Serum creatinine ≥2 Albumin ≥4 Anemia (hematocrit ≥35) High WBC count (N11,000) Platelets count ≥350,000 cell/cubic ml
U
N
C
t3:4
Open OR (95% CI)
p-Value
1.1 (0.73–1.61) 0.85 (0.59–1.22) 1.35 (0.92–1.97) 4.1 (1.38–12.45) 1.1 (0.76–1.52) 1.46 (0.72–2.81) 1.71 (0.9–3.1) 1.03 (0.74–1.44) 3.86 (1.53–9.6) 1.92 (1.01–3.54) 3.43 (1.44–8.16) 4.05 (0.94–21.12) 1.27 (0.91–1.78) 2.57 (1.31–4.95) 0.8 (0.32–2.33) 0.98 (0.4–2.84) 1.6 (0.66–4.64) 1.41 (0.71–2.71) 0.70 (0.44–1.14) 0.45 (1.39–3.53) 2.23 (0.7–1.53) 1.04 (0.7–1.53)
0.65 0.37 0.12 0.01 0.65 0.26 0.08 0.86 0.003 0.04 0.005 0.069 0.16 0.005 0.64 0.96 0.33 0.38 0.14 0.007 0.83 0.83
19 (0.7%) 15 (1%) 4 (0.3%) 282 (10%) 234 (16%) 48 (3%) 118 (4%) 81 (6%) 37 (3%) 14 (0.5%) 13 (1%) 1 (0.7%) 38 (1%) 24 (2%) 14 (1%) 56 (2%) 40 (3%) 16 (1%) 167 (6%) 130 (9%) 37 (3%) 348 (12%) 275 (19%) 73 (5%) 53 (2%) 35 (2%) 18 (1%) 3.2 4.8 1.5 0.15 0.24 0.05 174
5 (1.5%) 5 (2%) 0 (0%) 58 (17%) 55 (23%) 3 (3%) 24 (7%) 23 (10%) 1 (1%) 9 (1%) 4 (2%) 0 (0%) 11 (3%) 11 (5%) 0 (0%) 4 (1%) 4 (2%) 0 (0%) 33 (9%) 30 (12%) 3 (3%) 72 (21%) 68 (28%) 4 (4%) 4 (1%) 4 (2%) 0 (0%) 4.3 5.3 2.0 0.22 0.31 0.04 186
0.11 0.18 0.59 b0.001 0.01 0.78 0.01 0.02 0.29 0.11 0.27 0.78 0.007 0.003 0.30 0.30 0.31 0.27 0.006 0.09 0.86 b0.001 0.001 0.55 0.35 0.45 0.24 0.03 0.61 0.001 0.007 0.13 0.47 0.007
6 (2%) 73 (21%) 106 (30%) 164 (47%)
0.18
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Renal complications
p-Value
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Non-surgical complications
African American n (%)
R O
Surgical complications
24 (0.8%) 20 (1.2%) 4 (0.3%) 340 (12.5%) 289 (17%) 51 (3%) 142 (4.4%) 104 (6%) 38 (2.4%) 18 (0.5%) 17 (1%) 1 (0.06%) 49 (1.5%) 35 (2%) 14 (0.9%) 60 (1.8%) 44 (2.6%) 16 (1%) 200 (6.2%) 160 (9.5%) 40 (2.6%) 420 (13%) 343 (20%) 77 (5%) 57 (1.8%) 39 (2%) 18 (1%)
White n (%)
P
Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy Overall Laparotomy Laparoscopy ≤60 min 61–120 min 121–180 min ≥180 min
D
Mortality
E
t2:4 t2:5 t2:6 t2:7 t2:8 t2:9 t2:10 t2:11 t2:12 t2:13 t2:14 t2:15 t2:16 t2:17 t2:18 t2:19 t2:20 t2:21 t2:22 t2:23 t2:24 t2:25 t2:26 t2:27 t2:28 t2:29 t2:30 t2:31 t2:32 t2:33 t2:34 t2:35 t2:36 t2:37 t2:38 t2:39 t2:40 t2:41 t2:42 t2:43
Total cohort
T
Variable
60 (2%) 708 (24%) 940 (32%) 1191 (41%)
C
t2:3
E
t2:1 t2:2
H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx
myocardial infarction (0% vs. 0.2%, p = 0.99) and peripheral nerve injury (0% vs. 0.1%). In multivariable logistic regression model after adjustment for all confounders including surgical complexity and associated morbidities, AA race was not an independent predictor of “any postoperative complications” for both laparotomy group (OR 1.1, 95% CI 0.73–1.61, p = 0.65, Table 3) and laparoscopic group (OR 1.43, 95% CI 0.80–2.45, p = 0.21, Table 4).
243 244
30-day postoperative mortality
251
No difference in 30-day mortality was found between AA and W patients for the entire cohort (1% vs. 1%, p = 0.11), laparoscopic group (0% vs. 0.3%, p = 0.59) and laparotomy group (2% vs. 1%, p = 0.18, Table 2). In multivariable logistic regression model, AA race was not
252 253
Table 4 Multivariate regression analysis for “any complication” within 30 days following laparoscopic surgery for endometrial cancer.
245 246 247 248 249 250
254 255 t4:1 t4:2 t4:3
Variable
OR (95% CI)
p-Value
t4:4
African American Cardiac comorbidities Hypertension ASA class 3 ASA class 4–5 Albumin ≥4 Anemia (hematocrit ≥35) High WBC count (N11,000)
0.55 (0.16–1.39) 2.03 (0.58–5.48) 0.1.36 (0.82–2.30) 1.29 (0.78–2.14) 2.02 (0.45–6.41) 2.49 (0.50–4.55) 0.35 (0.20–0.67) 1.57 (0.53–3.76)
0.26 0.20 0.24 0.32 0.28 0.38 0.0008 0.35
t4:5 t4:6 t4:7 t4:8 t4:9 t4:10 t4:11 t4:12
Please cite this article as: Mahdi H, et al, Racial disparity in the 30-day morbidity and mortality after surgery for endometrial cancer, Gynecol Oncol (2014), http://dx.doi.org/10.1016/j.ygyno.2014.05.024
H. Mahdi et al. / Gynecologic Oncology xxx (2014) xxx–xxx
272 273 274 275 276 277 278 279 280 281 282 283 284 285 286 287 288 289 290 291 292 293 294 295 296 297 298 299 300 301 302 303 304 305 306 307 308 309 310 311 312 313 314 315 316 317 318 319
C
270 271
E
Conflict of interest
353
All authors declare no conflict of interest. Funding
354 355
No funding source.
356
Uncited references
357 Q7
F
268 269
R
266 267
R
264 265
N C O
262 263
U
260 261
O
In this study using the ACS-NSQIP database, we found that African American patients with endometrial cancer were more likely to have higher levels of preoperative morbidities, and less likely to have minimally invasive surgery. African American patients had higher rates of postoperative complications following surgical staging for endometrial cancer compared to their white counterpart. Both surgical and nonsurgical complications were significantly higher in African American patients. Among non-surgical complications, only infectious and pulmonary complications were significantly higher among African American compared to white patients, while no significant difference was found in the rate of cardiac and renal complications between the two racial groups. On the other hand, in multivariate analysis after adjusting for pre-operative morbidities and surgical complexity, African American race was not an independent predictor of adverse 30-day postoperative outcome following surgery for endometrial cancer. As one of the largest multihospital studies to examine risks for developing adverse operative outcomes after cancer surgery across the two racial groups, our results suggest that the 30-day postoperative outcome after endometrial cancer surgery in African American women is comparable to their white counterpart when controlling for preoperative morbidities and surgical complexity. Prior reports on racial disparities of short-term postoperative outcomes in endometrial cancer are limited. Parsons et al. reported no difference in the rate of 30-day postoperative outcomes in racial minority patients undergoing cancer at ACS-NSQIP hospitals compared to white patients [17]. In this study, African American patients were more likely to have pre-operative morbidities compared to white patients. Some of these pre-operative morbidities were significantly associated with adverse postoperative outcome in multivariate analysis like ascites, preoperative weight loss (10% within 6 months), neurologic comorbidities and anemia. These findings might explain at least partially the observed difference in short term postoperative outcome between the two racial groups. Therefore, it is important to focus on managing these morbidities prior to surgery in order to minimize postoperative complications. Minimally invasive surgery has been recently introduced in managing endometrial cancer patients. It is well established that minimally invasive surgery is associated with less peri-operative complications, shorter hospital stay and faster recovery [18,19]. Interestingly, African American patients were less likely to undergo minimally invasive surgery compared to their white counterpart. This could be related to higher frequency of pre-operative comorbidities in African American patients and possibly other socio-economic factors. On the other hand, no difference in surgical complexity was found between the two racial groups. Therefore, increasing the likelihood of minimally invasive approach might help decrease the risk of postoperative complications in this patient population. In this study, other independent predictors of adverse postoperative morbidity after laparotomy for endometrial cancer included surgical complexity, neurologic comorbidities, ascites, pre-operative weight loss (10% within 6 months), anemia, leukocytosis and higher ASA class. Previous studies have identified risk factors for post-operative complications following surgical treatment of endometrial cancer, including older age, obesity (BMI ≥50), preoperative WBC count, higher ASA class, laparotomy and surgical complexity [19,20]. Additionally, renal insufficiency (preoperative creatinine N 1.5 mg/dL) and hypoalbuminemia are associated with more postoperative complications and are independent risk factors of postoperative complications following surgical treatment of gynecologic malignancies [20,21]. Therefore, the higher rate of postoperative complications noticed in univariate analysis in African American women with endometrial cancer could be attributed to the greater number of preoperative comorbidities in these patients.
R O
259
P
Discussion
320 321
D
258
Although our study provides insight into the short-term operative outcomes across the two racial groups in ACS NSQIP, we acknowledge several limitations. First, we lacked information on patients' socioeconomic and insurance status, which have been shown to correlate with race. Alternatively, it is also possible that African American patients treated within ACS NSQIP hospitals are carriers of a more favorable health care coverage when compared with other patients who typically cluster at lower-quality hospitals. Second, we did not adjust for surgeon or hospital volume, which has been associated with surgical outcomes. Third, our results were not adjusted for stage at cancer diagnosis, which typically impacts use of effective cancer care and overall survival outcomes. However, we adjusted for extent of surgical treatment, which can act as a proxy for extent of cancer. Despite these limitations, we present evidence of relatively comparable short-term operative outcomes across the two racial groups from more than 250 qualityseeking hospitals that go beyond mortality to examine other important short-term operative outcomes. Ultimately, African American race was not independently associated with a greater risk for postoperative complications or mortality following endometrial cancer surgery. The propensity for African American patients to experience complications is only seen on univariate analysis and likely reflects their preoperative comorbidities as well as the likelihood that they undergo an open staging procedure. Therefore, more efforts should be directed to optimally manage the preoperative comorbidities in this patient population in order to achieve postoperative outcome equivalent to their white counterpart. Further, increasing the likelihood of performing minimally invasive surgery in African American patients with endometrial cancer should be considered if appropriate to decrease the rate of postoperative complications. Further research should be directed to identify the factors contributing to having higher rates of pre-operative comorbidities and lower likelihood of minimally invasive surgery in African American patients with endometrial cancer.
E
an independent predictor of 30-day postoperative mortality for the entire cohort (OR 1.4, 95% CI 0.46–3.8, p = 0.48).
T
256 257
5
[14,15]
322 323 324 325 326 327 328 329 330 331 332 333 334 335 336 337 338 339 340 341 342 343 344 345 346 347 348 349 350 351 352
358
References
359
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