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. Author manuscript; available in PMC: 2022 Nov 1.
Published in final edited form as: Ann Surg Oncol. 2021 May 6;28(12):7795–7806. doi: 10.1245/s10434-021-10086-y

Differences in Sociodemographic Disparities in Patients Undergoing Surgery for Advanced Colorectal and Ovarian Cancer

Ellen M Goldberg 1, Yaniv Berger 2, Divya Sood 2, Katherine C Kurnit 3, Josephine S Kim 3, Nita K Lee 3, S Diane Yamada 3, Kiran K Turaga 2, Oliver S Eng 2
PMCID: PMC8530985  NIHMSID: NIHMS1720567  PMID: 33959831

Abstract

Background:

Cytoreductive surgery (CRS) for ovarian cancer with peritoneal metastases (OPM) is an established treatment, yet access-related racial and socioeconomic disparities are well documented. CRS for colorectal cancer with peritoneal metastases (CRPM) is garnering more widespread acceptance, and it is unknown what disparities exist with regards to access.

Methods:

This retrospective cross-sectional multicenter study analyzed medical records from the National Cancer Database from 2010–2015. Patients diagnosed with CRPM or ORP only and either no resection or confirmed resection were included. Patient-level and facility-level characteristics were analyzed using univariate and multivariable logistic regressions to identify associations to receipt of CRS.

Results:

A total of 6,634 patients diagnosed with CRPM and 14,474 diagnosed with OPM were included in this study. Among patients with CRPM, 18.1% underwent CRS. In the multivariable analysis, female gender (odds ratio [95% CI]; 2.04 [1.77—2.35]; P<.001) and treatment at an academic or research facility (OR 1.55 [1.17—2.05]; P=.002) were associated with CRS. Among patients with OPM, 87.1% underwent CRS. In the multivariable analysis, treatment at facilities with higher-income patient populations was positively associated with CRS, while age (OR 0.97 [0.96—0.98]; P<.001), use of non-private insurance (OR 0.69 [0.56—0.85]; P=.001), and listed as Black (OR 0.62 [0.45—0.86]; P=.004) were negatively associated with CRS.

Conclusion:

There were more systemic barriers to CRS for patients with OPM than for patients with CRPM. As CRS becomes more widely practiced for CRPM, it is likely that more socioeconomic and demographic barriers will be elucidated.

Introduction

In 2017, there were over 200,000 new cases of colorectal cancer (CRC) in the United States alone.1 At the time of diagnosis, 22% of patients with colorectal cancer have metastatic disease, and 30% to 40% of patients treated with curative intent develop recurrent, typically metastatic disease.2,3 There have been significant developments and progress in the management of metastatic CRC throughout the past several decades, and evaluation for resection of hepatic and pulmonary metastases has evolved to become a part of the treatment algorithm.4 4% of patients with metastatic CRC present with their first and only metastasis in the peritoneum, and colorectal cancer peritoneal metastases (CRPM) are the second leading cause of death and affect up to 30% of patients with CRC. 5–8 Surgical management of CRPM is rapidly emerging, and recent data from the PRODIGE 7 trial supports cytoreductive surgery as the standard of therapy and complete resection as the most important factor determining survival following treatment.9

Complex procedures for advanced CRC require significant institutional expertise and resources.5,10–12 In surgical removal of hepatic metastases among patients with CRC, demographic and socioeconomic differences have been shown to exist in both the patients and the treating facilities. After controlling for patient and tumor characteristics, academic facilities and facilities that serve a greater percentage of patients from high-income catchment areas are more likely to perform surgical removal of colorectal liver metastases.10

Alternatively, cytoreductive surgery of metastatic ovarian cancer in the peritoneum has been established as a beneficial treatment since the 1980s.13,14 Racial disparities in access to advanced treatments for ovarian cancer are well documented; while some studies have shown comparable clinical outcomes when Black patients receive identical treatment as white patients, 15,16 Black patients are less likely to receive the same standard of care.16–24 Current literature describing disparities in survival between Black and white patients with ovarian cancer are mixed; some studies demonstrate similar mortality rates,17,25 while others report significant disparities in disease-specific and all-cause mortality.16,18,19,26,27 High volume centers and surgery with specialty trained gynecologic oncology surgeons remains a quality standard but can be limited to patients with the resources to access these facilities, and patients who attend hospitals with lower case volume are less likely to receive care that adheres to National Comprehensive Cancer Network guidelines.16,23,28,29 Over the last decade, studies have consistently shown Black, lower socioeconomic status (SES), and non-privately insured patients to be less likely to receive “guideline-adherent treatment.”16–24

The purpose of this study was to examine the disparities in surgical resection rates of peritoneal metastases for patients with advanced colorectal and ovarian cancer separately and illustrate the differences in disparities between the two patient populations. We hypothesized that in two independent analyses, there would be significantly fewer demographic, socio-economic, and facility-level barriers to surgical intervention for patients with ovarian cancer due to the accepted quality standards, prior research demonstrating benefit to cytoreductive surgery, and institutional knowledge and expertise gained over the last four decades in comparison to patients with CRC.

Materials and Methods:

We conducted retrospective cross-sectional studies of patients with CRPM and patients with ovarian cancer with peritoneal metastases separately using the National Cancer Data Base (NCDB). The NCDB is a nationwide and facility-based prospective clinical oncology database jointly sponsored by the Commission on Cancer of the American College of Surgeons and the American Cancer Society. Established in 1989, the NCDB consists of data sourced from over 1,500 Commission on Cancer-accredited facilities, capturing over 70% of incident cancer diagnoses across the United States. Data are de-identified and compliant with Health Insurance Portability and Accountability Act (HIPPA), and this study was deemed to be IRB exempt.

Patients diagnosed with colorectal adenocarcinoma with peritoneal metastases

1,294,632 patients diagnosed with CRC in the NCDB from 2010 to 2015 were initially identified. 1,218,148 patients were diagnosed with adenocarcinoma and of those, 112,486 with stage IV disease. The NCDB explicitly reports the presence of disease in the liver, lung, brain, and bone, and patients with disease in any of these locations were excluded, leaving 8,593 patients. In order to approximate receipt of cytoreductive surgery for peritoneal disease, patients either with no resection or confirmed resection at a distant site only were included in the final dataset. Of these 7,326 patients, an additional 692 patients were excluded due to missing information. The final 6,634 patients represent all patients diagnosed with stage IV colorectal adenocarcinoma with peritoneal metastases, defined by the study authors based on the exclusion of liver, lung, brain, or bone metastases.

Patients diagnosed with ovarian cancer with peritoneal metastases

All patients in the NCDB diagnosed with ovarian cancer from 2010 to 2015 were initially included, totaling 211,937 patients. 176,827 patients remained after selecting for specific histologies including carcinoma, adenocarcinoma, mucinous adenocarcinoma, mucinous cystadenoma, and serous carcinoma, and 30,833 patients after selecting those diagnosed with peritoneal metastases beyond the pelvis. Only cases that reported either no surgery or cytoreductive surgery were included, leaving 21,627 patients. After removing cases that reported a distant metastasis beyond the peritoneum, 15,481 patients remained, and of these, an additional 1,007 patients were excluded due to missing information. The final 14,474 patients represent all patients diagnosed with stage IIIB or IIIC ovarian cancer with only peritoneal metastases.

Study covariates

Individual patient-level characteristics included age, sex, race (Black, white, or other), ethnicity (Hispanic or non-Hispanic), insurance status (private, other insurance, or uninsured), and receipt of treatment at multiple facilities. Data describing the patient’s location of residence were also extracted, generalized to a zip-code using census data including median income quartile, percent of residents without a high school diploma, and distance to the treating facility defined as linear distance between the facility and the center of the patient’s reported zip code, or city if zip code is not available. Distance to treatment facility was converted into a binary variable with a cut-off value of 50 km.10 The median income quartile variable from 2012–2016 was used, and missing values were replaced with the next closest year if available. Facility-level variables included facility type (community cancer center, comprehensive community cancer center, academic or research facility, and integrated facility) and facility income quartile (FIQ), a variable generated using the proportion of patients from the highest income quartile treated at each facility. The outcome variable was surgical resection of CRPM as described above, and cytoreductive surgery in the peritoneum for patients with ovarian cancer.

Statistical Analysis

All statistical analyses were conducted using STATA software (version 16.1; StataCorp LLC, College Station, Texas). All tests were two-sided with a significance level of α = 0.05.

First, patient-level and facility-level characteristics were compared across surgery status separately for patients with CRPM and patients with ovarian cancer using chi-square, ANOVA, and ranksum tests where appropriate and adjusted for multiple comparisons using a Bonferroni correction. Variables that had a p value equivalent to 0.20 or lower after adjusting for multiple comparisons were included in a multivariable logistic regression model for cytoreductive surgery using a generalized estimating equation with cluster analysis by facility to account for intra-facility correlation. For patients with CRC, these variables included age, sex, insurance status, distance to treatment facility, TNM T and N classifications, margins of the primary tumor resection, facility type, treatment at multiple facilities, and receipt of systemic therapy. For patients with ovarian cancer, age, race, zip code median income quartile, insurance status, zip code percent without a high school diploma quartile, distance to treatment facility, TNM T and N classifications, Charlson-Deyo Comorbidity score, facility type, FIQ, treatment at multiple facilities, and receipt of systemic therapy were included. TNM staging and primary tumor resection were included to adjust for tumor-related impact on course of treatment. Lastly, univariate comparisons between proportions of sociodemographic characteristics between facility types and between FIQs were also determined using ANOVA or ranksum tests where appropriate and adjusted for multiple comparisons.

Results

Comparison of Resected and Unresected Patients with Peritoneal Metastases

Patient characteristics among patients with colorectal cancer

Of the 6,634 patients in the NCDB between 2010–2015 diagnosed with stage IV CRPM, 1,201 (18.1%) underwent cytoreductive surgery. Additional patient characteristics are shown in Table 1. The median age of patients who underwent cytoreductive surgery versus those who did not was lower (63 vs. 67, p < 0.0001), and lower resection rates were noted among males when compared to females (12.7% vs. 23.3%, p < 0.0001). Patients with Medicare, Medicaid, or other non-private insurance also had lower rates of surgery when compared to patients with private insurance (16.3% vs. 27.2%, p < 0.0001). Patients treated at multiple facilities had a higher rate of cytoreductive surgery (24.0% vs. 17.5%, p < 0.0001), as did patients with receipt of systemic therapy and patients who lived farther than 50 km from their initial treatment facility (29.2% vs. 10.6%, p < 0.0001; and 26.4% vs. 21.2%, p = 0.0070, respectively).

Table 1:

Demographics of Patients with Colorectal Cancer with Peritoneal Metastases by Receipt of Cytoreductive Surgery (CRS)

Characteristic Did Not Undergo CRS
N = 5,433 (81.9%)		 Underwent CRS
N = 1,201 (18.1%)		 P
Age (IQR), y 67 (58 – 77) 63 (54 – 74) <0.0001*
Sex
  Male 2829 (52.1) 412 (34.3)
  Female 2604 (47.9) 789 (65.7) <0.0001*
Race
  White 4531 (83.4) 998 (83.1)
  Black 680 (12.5) 160 (13.3) 0.49
  Other 222 (4.1) 43 (3.6) 0.45
Ethnicity
  Non-Hispanic 5148 (94.8) 1147 (95.5)
  Hispanic 285 (5.2) 54 (4.5) 0.29
Median income quartile
  Quartile 1 1127 (20.7) 227 (18.9) 0.079
  Quartile 2 1260 (23.2) 276 (23)
  Quartile 3 1386 (25.5) 303 (25.2)
  Quartile 4 1660 (30.6) 395 (32.9)
Insurance status
  Private 1768 (32.5) 481 (40)
  Other insurance 3399 (62.6) 664 (55.3) <0.0001*
  Uninsured 266 (4.9) 56 (4.7) 0.099
% without high school diploma quartile
  Quartile 1 1232 (22.7) 248 (20.6) 0.28
  Quartile 2 1453 (26.7) 337 (28.1)
  Quartile 3 1608 (29.6) 352 (29.3)
  Quartile 4 1140 (21) 264 (22)
Distance to facility
  ≤ 50 km 4520 (83.2) 960 (79.9) 0.007
  > 50 km 913 (16.8) 241 (20.1)
T classification
  1 237 (4.4) 32 (2.7) <0.0001*
  2 69 (1.3) 12 (1)
  3 513 (9.4) 108 (9)
  4 1122 (20.7) 184 (15.3)
  X 3492 (64.3) 865 (72)
N classification
  0 2257 (41.5) 493 (41) <0.0001*
  1–2 1207 (22.2) 233 (19.4)
  X 1969 (36.2) 475 (39.6)
Surgical resection margins of primary tumor
  Negative 1808 (33.3) 643 (53.5)
  Positive 1118 (20.6) 312 (26) <0.0010*
  Unknown/NA 2507 (46.1) 246 (20.5)
Charlson-Deyo Comorbidity Score
  0 3815 (70.2) 868 (72.3) 0.16
  1 1170 (21.5) 251 (20.9)
  2 301 (5.5) 56 (4.7)
  3 147 (2.7) 26 (2.2)
Facility type
  Comm center 637 (11.7) 101 (8.4) 0.0004*
  Comp comm 2342 (43.1) 492 (41)
  Academic 1649 (30.4) 422 (35.1)
  Integrated 805 (14.8) 186 (15.5)
FIQ (% of patients from high-income zip codes)
  Quartile 1 1449 (26.7) 257 (21.4) 0.033
  Quartile 2 917 (16.9) 230 (19.2)
  Quartile 3 1829 (33.7) 441 (36.7)
  Quartile 4 1238 (22.8) 273 (22.7)
Treated at multiple facilities 471 (8.7) 149 (12.4) <0.0001*
Receipt of systemic therapy 2039 (37.5) 840 (69.9) <0.0001*
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Abbreviations: CRS, cytoreductive surgery; Comm center, community cancer center; Comp comm, comprehensive community cancer center; NA, not available

*

signifies statistically significant at p < 0.05, adjusted for multiple comparisons

Patient characteristics among patients with ovarian cancer

15,507 patients in the NCDB were diagnosed with stage IIIB or IIIC ovarian cancer with peritoneal metastases from 2010 to 2015, 13,508 (87.1%) of whom underwent cytoreductive surgery. Additional characteristics for patients with ovarian cancer are displayed in Table 2. Patients who underwent cytoreductive surgery were younger than those who did not (median age: 64 vs. 75, p < 0.0001). Lower resection rates were noted among Black patients when compared to white patients (80.8% vs. 87.4%, p < 0.0001) and patients insured with Medicare, Medicaid, other non-private insurance, or were uninsured when compared to patients with private insurance (94.5% vs. 81.5%; p < 0.0001). An area of residence within the two highest income quartiles was also associated with higher rates of surgery (87.8% vs. 85.5%; p < 0.0001).

Table 2:

Demographics of Patients with Ovarian Cancer with Peritoneal Metastases by Receipt of Cytoreductive Surgery

Characteristic Did Not Undergo CRS
N = 1,880 (13.0%)		 Underwent CRS
N = 12,594 (87.0%)		 P
Age (IQR), y 75 (66 – 82) 64 (56 – 71) < 0.0001*
Race
  White 1625 (86.4) 11230 (89.2)
  Black 193 (10.3) 812 (6.4) < 0.0001*
  Other 62 (3.3) 552 (4.4) 0.063
Ethnicity
  Non-Hispanic 1780 (94.7) 11940 (94.8)
  Hispanic 100 (5.3) 654 (5.2) 0.82
Median income quartile
  Quartile 1 350 (18.6) 1788 (14.2) < 0.0001*
  Quartile 2 409 (21.8) 2702 (21.5)
  Quartile 3 466 (24.8) 3305 (26.2)
  Quartile 4 655 (34.8) 4799 (38.1)
Insurance status
  Private 340 (18.1) 5817 (46.2)
  Other insurance 1496 (79.6) 6437 (51.1) < 0.0001*
  Uninsured 44 (2.3) 340 (2.7) < 0.0001*
% without high school diploma quartile
  Quartile 1 334 (17.8) 1873 (14.9) < 0.0001*
  Quartile 2 511 (27.2) 3059 (24.3)
  Quartile 3 561 (29.8) 4042 (32.1)
  Quartile 4 474 (25.2) 3620 (28.7)
Distance to facility
  ≤ 50 km 1499 (79.7) 8737 (69.4) < 0.0001*
  > 50 km 381 (20.3) 3857 (30.6)
T classification
  1 2 (.1) 290 (2.3) < 0.0001*
  2 6 (.3) 448 (3.6)
  3 1757 (93.5) 7055 (56)
  X 115 (6.1) 4801 (38.1)
N classification
  0 1286 (68.4) 7789 (61.8) < 0.0001*
  1–2 287 (15.3) 1647 (13.1)
  X 307 (16.3) 3158 (25.1)
Charlson-Deyo Comorbidity Score
  0 1295 (68.9) 10084 (80.1) < 0.0001*
  1 374 (19.9) 2060 (16.4)
  2 146 (7.8) 348 (2.8)
  3 65 (3.5) 102 (.8)
Facility type
  Comm center 130 (6.9) 338 (2.7) < 0.0001*
  Comp comm 769 (40.9) 4785 (38)
  Academic 683 (36.3) 5440 (43.2)
  Integrated 298 (15.9) 2031 (16.1)
FIQ (% of patients from high-income zip codes)
  Quartile 1 287 (15.3) 790 (6.3) < 0.0001*
  Quartile 2 529 (28.1) 4046 (32.1)
  Quartile 3 635 (33.8) 5050 (40.1)
  Quartile 4 429 (22.8) 2708 (21.5)
Treated at multiple facilities 197 (10.5) 2146 (17) < 0.0001*
Receipt of systemic therapy 149 (7.9) 11326 (89.9) < 0.0001*
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Abbreviations: CRS, cytoreductive surgery; Comm center, community cancer center; Comp comm, comprehensive community cancer center; NA, not available

*

signifies statistically significant at p < 0.05, adjusted for multiple comparisons

Multivariable Analysis

Multivariable analysis among patients with colorectal cancer

In the multivariable analysis among patients with CRPM (Table 3), female gender (odds ratio [OR] 2.04 [95% CI 1.77 – 2.35]) and treatment at an academic facility (OR 1.55 [1.17 – 2.05]) were associated with surgical resection (p < 0.05) after adjusting for receipt of chemotherapy and primary tumor staging and resection margin. Age was negatively associated with surgical resection (OR 0.99 [0.98 – 0.99]), and treatment at multiple facilities and insurance status were not found to be associated with surgical resection.

Table 3:

Factors Correlating with Cytoreductive Surgery in Patients with Colorectal Cancer with Peritoneal Metastases

Characteristic Univariate OR (95% CI) P Multivariable OR (95% CI) P
Age (IQR), y 0.98 (0.97 – 0.98) < 0.001 0.99 (0.98 – 0.99) < 0.001
Sex
  Male Reference -- Reference --
  Female 2.08 (1.82 – 2.37) < 0.001 2.04 (1.77 – 2.35) < 0.001
Insurance status
  Private Reference -- Reference --
  Other insurance 0.72 (0.63 – 0.82) < 0.001 1.05 (0.89 – 1.24) 0.57
  Uninsured 0.77 (0.57 – 1.05) 0.10 0.90 (0.64 – 1.27) 0.55
Distance to facility
  ≤ 50 km Reference -- Reference --
  > 50 km 1.24 (1.06 – 1.46) 0.007 1.04 (0.88 – 1.24) 0.65
T classification
  1 Reference -- Reference --
  2 1.29 (0.63 – 2.63) 0.49 1.02 (0.49 – 2.14) 0.95
  3 1.56 (1.02 – 2.38) 0.040 1.42 (0.89 – 2.26) 0.14
  4 1.21 (0.81 – 1.81) 0.34 1.29 (0.83 – 2.01) 0.27
  X 1.83 (1.26 – 2.67) 0.002 1.69 (1.11 – 2.58) 0.014
N classification
  0 Reference -- Reference --
  1–2 0.88 (0.75 – 1.05) 0.16 0.80 (0.66 – 0.98) 0.027
  X 1.10 (0.96 – 1.27) 0.16 1.01 (0.86 – 1.18) 0.95
Surgical resection margins of primary tumor
  Negative -- Reference --
  Positive 0.78 (0.67 – 0.92) 0.002 0.81 (0.68 – 0.96) 0.017
  Unknown/NA 0.28 (0.24 – 0.32) < 0.001 0.48 (0.38 – 0.61) < 0.001
Facility type
  Comm center -- Reference --
  Comp comm 1.32 (1.05 – 1.67) 0.017 1.23 (0.94 – 1.61) 0.13
  Academic 1.61 (1.28 – 2.04) < 0.001 1.55 (1.17 – 2.05) 0.002
  Integrated 1.46 (1.12 – 1.90) 0.005 1.28 (0.94 – 1.74) 0.12
Treated at multiple facilities 1.49 (1.23 – 1.81) < 0.001 1.17 (0.94 – 1.46) 0.160
Receipt of systemic therapy 3.87 (3.38 – 4.43) < 0.001 2.61 (2.13 – 3.20) < 0.001
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Abbreviations: Comm center, community cancer center; Comp comm, comprehensive community cancer center; NA, not available

Multivariable analysis among patients with ovarian cancer

Results of the multivariable analysis among patients with ovarian cancer are displayed on Table 4. After adjusting for primary tumor staging and receipt of chemotherapy, age (OR 0.97 [95% CI 0.96 – 0.98]), use of Medicare, Medicaid, or other non-private insurance (OR 0.69 [0.56 – 0.85]), and patients listed as Black (OR 0.62 [0.45 – 0.86]) were negatively associated with cytoreductive surgery (p < 0.05). Patients who lived farther away (OR 1.82 [1.44 – 2.31]) and treatment at a higher FIQ facility (2nd quartile: OR 2.08 [1.42 – 3.03]; 3rd quartile: OR 2.31 [1.58 – 3.38]; 4th quartile: OR 1.94 [1.29 – 2.92]) were positively associated with cytoreductive surgery.

Table 4:

Factors Correlating with Cytoreductive Surgery in Patients with Ovarian Cancer with Peritoneal Metastases

Characteristic Univariate OR (95% CI) P Multivariable OR (95% CI) P
Age (IQR), y 0.92 (0.91 – 0.92) < 0.001 0.97 (0.96 – 0.98) < 0.001
Race
  White Reference -- Reference --
  Black 0.61 (0.52 – 0.72) < 0.001 0.62 (0.45 – 0.86) 0.004
  Other 1.29 (0.99 – 1.68) 0.064 1.19 (0.79 – 1.79) 0.40
Median income quartile -- --
  Quartile 1 Reference Reference
  Quartile 2 1.29 (1.11 – 1.51) 0.001 1.34 (1.03 – 1.74) 0.029
  Quartile 3 1.39 (1.19 – 1.61) < 0.001 1.31 (0.98 – 1.73) 0.065
  Quartile 4 1.43 (1.25 – 1.65) < 0.001 1.24 (0.90 – 1.71) 0.20
Insurance status
  Private Reference -- Reference --
  Other insurance 0.25 (0.22 – 0.28) < 0.001 0.69 (0.56 – 0.85) 0.001
  Uninsured 0.45 (0.32 – 0.63) < 0.001 0.62 (0.34 – 1.02) 0.059
% without high school diploma quartile
  Quartile 1 Reference -- Reference --
  Quartile 2 1.07 (0.92 – 1.24) 0.39 0.72 (0.55 – 0.94) 0.016
  Quartile 3 1.28 (1.11 – 1.49) 0.001 0.80 (0.59 – 1.09) 0.16
  Quartile 4 1.36 (1.17 – 1.58) < 0.001 0.78 (0.55 – 1.10) 0.16
Distance to facility
  ≤ 50 km Reference -- Reference --
  > 50 km 1.74 (1.54 – 1.96) < 0.001 1.82 (1.44 – 2.31) < 0.001
T classification
  1 Reference -- Reference --
  2 0.51 (0.10 – 2.57) 0.42 0.57 (0.093 – 3.54) 0.55
  3 0.028 (0.0069 – 0.11) < 0.001 0.035 (0.0071 – 0.18) < 0.001
  X 0.29 (0.071 – 1.17) 0.082 0.47 (0.09 – 2.39) 0.36
N classification
  0 Reference -- Reference --
  1–2 0.95 (0.82 – 1.09) 0.45 1.13 (0.90 – 1.41) 0.28
  X 1.70 (1.49 – 1.94) < 0.001 0.68 (0.54 – 0.86) 0.001
Charlson-Deyo Comorbidity Score
  0 Reference -- Reference --
  1 0.71 (0.62 – 0.80) < 0.001 0.86 (0.70 – 1.05) 0.13
  2 0.55 (0.50 – 0.61) < 0.001 0.47 (0.34 – 0.66) < 0.001
  3 0.59 (0.53 – 0.65) < 0.001 0.35 (0.19 – 0.64) 0.001
Facility type
  Comm center Reference -- Reference --
  Comp comm 2.39 (1.93 – 2.97) < 0.001 1.62 (1.07 – 2.45) 0.023
  Academic 3.06 (2.46 – 3.81) < 0.001 1.41 (0.92 – 2.18) 0.20
  Integrated 2.62 (2.07 – 3.32) < 0.001 1.23 (0.77 – 1.97) 0.38
FIQ (% of patients from high-income zip codes)
  Quartile 1 Reference -- Reference --
  Quartile 2 2.60 (2.22 – 3.05) < 0.001 2.08 (1.42 – 3.03) < 0.001
  Quartile 3 2.91 (2.48 – 3.40) < 0.001 2.31 (1.58 – 3.38) < 0.001
  Quartile 4 2.66 (2.21 – 3.20) < 0.001 1.94 (1.29 – 2.92) 0.002
Treated at multiple facilities 1.75 (1.50 – 2.05) < 0.001 1.09 (0.88 – 1.35) 0.45
Receipt of systemic therapy 103.8 (86.93 – 123.87) < 0.001 92.92 (74.55 – 115.82) < 0.001
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Abbreviations: Comm center, community cancer center; Comp comm, comprehensive community cancer center; NA, not available

Facility-Level Characteristics

Facility types among patients with colorectal cancer

In this study, 1,182 facilities treated patients with CRPM, 24.4% of which were designated as community cancer centers, 41.7% as comprehensive community cancer centers, 18.6% as academic or research facilities, and 15.3% as integrated centers. Patients treated at academic facilities had higher rates of surgical resection when compared to other facility types (20.4% vs. 17.1%, p = 0.001). Academic facilities treated 31.2% of the patient population, and when compared to all other facility types were more likely to treat younger patients, patients with private insurance (37.1% vs. 32.1%, p = 0.0002), and non-white patients (22.2% vs. 14.1%, p < 0.0001) (eTable 1). Academic facilities were also more likely to be a high FIQ facility (29.3% are in the highest FIQ compared to 19.8% in other facilities, p < 0.0001).

Facility types among patients with ovarian cancer

1,040 different facilities treated patients with ovarian cancer, 18.8% of which were designated as community cancer centers, 44.9% as comprehensive community cancer centers, 20.8% as academic or research facilities, and 15.6% as integrated centers. Patients who were treated at facilities in the highest FIQ were more likely to undergo cytoreductive surgery when compared to facilities in the lowest FIQ (86.3% vs. 73.4%; p < 0.0001), as were patients treated at academic facilities when compared to all other facilities (88.8% vs. 85.7%; p < 0.0001).

Facilities in the two highest FIQs treated younger patients, more patients with private insurance (45.5% vs. 37.9%, p < 0.0001), and were more likely to be academic facilities (46.6% vs. 35.6%, p < 0.0001) (eTable 1). Patients with private insurance were more likely to undergo cytoreductive surgery across all FIQs (eFigure 1), and when comparing patients from zip codes with similar income quartiles, those who attended low FIQ facilities were less likely to undergo cytoreductive surgery than those who had surgery at facilities in the top three quartiles (eFigure 2).

Discussion

In this study, cytoreductive surgery for peritoneal metastases from colorectal and ovarian cancer were examined in relation to patient and facility-level characteristics. Cytoreductive surgery for CRPM is a complex procedure requiring extensive institutional expertise and resources.5 The current study did not identify any SES variables (notably race, insurance type, or median zip code income quartile) as correlating with rate of surgery among patients with CRC. However, academic facilities were found to be associated with a higher likelihood of undergoing surgery and were more likely to be higher FIQ institutions. Reasons for this could be that cytoreductive surgery among patients with CRPM has been less widely practiced due to its novelty, complexity, and required expertise, and thus more often performed at facilities equipped with multidisciplinary teams and extensive resources. In fact, recent data have demonstrated that the majority of cytoreductive surgeries are performed at academic or academic-affiliated institutions across the country.30 Other studies have shown that academic facilities are more likely to offer access to treatment of metastatic disease, and that multidisciplinary collaborations are positively associated with overall survival and treatment decision-making specifically in patients with stage III CRC.10,31,32 It is reasonable to infer that these advantages apply similarly to the even more complex care of patients with stage IV CRC. Patients who attended academic facilities were more likely to benefit from multidisciplinary collaborations and improved treatment.

Previously documented socioeconomic and racial disparities in ovarian cancer treatment were evident in this study despite the institutional knowledge and expertise gained from four decades of cytoreductive surgery as the accepted standard of care; Black patients and patients without private insurance were significantly less likely to undergo cytoreductive surgery. The effects of racism on health through the systemic and unjust distribution of socioeconomic resources, discrimination, and the ensuing psychosocial stress have been thoroughly documented. 33,34 As a result, Black patients are less likely to benefit when advances in medical treatment occur. Link and Phelan seek to explain this phenomenon via the “fundamental cause theory”, hypothesizing that, in addition to and independently of SES, racism functions as a fundamental cause of disease due to inequalities in power, resources, and prestige limiting access to important resources and innovations.35,36 As a result, diseases that are more amenable to treatment are more likely to demonstrate disparities in access and outcomes. This has been demonstrated in both cross-sectional studies across diseases of varying amenability25,37 and temporally during the introduction of new treatments.38,39 Terplan et al (2012) showed that the racial disparity in survival among patients with ovarian cancer increased over time – a reflection of treatment disparities – appearing after cytoreductive surgery and platinum-based chemotherapy became standards of care.18 The results of this study were no exception, showing that Black patients diagnosed with peritoneal metastatic ovarian cancer were less likely to undergo cytoreductive surgery.

In addition to racial discrimination, lower SES was also shown to have harmful consequences.35 Previous studies have demonstrated that patient travel and a multi-facility care regimen were associated with an increased likelihood of treatment in other complex oncologic procedures.10,40,41 This study showed that increased distance traveled, treatment at multiple facilities, and treatment at higher FIQ facilities correlated to increased likelihood of cytoreductive surgery, while patients who were not privately insured were less likely to undergo surgical resection. These findings suggest that disparities in independent financial resources and knowledge of which institutions to receive care may contribute to differences in surgical resection rates. However, patients who attended the lowest FIQ facilities had lower rates of cytoreductive surgery regardless of median zip code income quartile, suggesting that individual assets were only beneficial when combined with the resources of higher FIQ facilities.

While no SES variables were found to be statistically significant in this analysis among patients with CRPM, we recognize that systems in place for treatment of CRC in general are far from equitable. For example, racial disparities in stage at diagnosis and survival among patients once diagnosed with CRC are well documented: incidence and mortality from CRC is highest among Black patients, and delayed diagnosis accounts for 60% of the difference in mortality.42–44 As cytoreductive surgery becomes accepted as the standard of care for CRPM, with increased availability of this procedure and development of more robust referral systems and awareness, assessment for surgical treatment of CRPM may become more commonplace. In following the fundamental cause theory, it is possible that other barriers to access will increase over time due to the socioeconomic and racial disparities present throughout healthcare in the United States. It is clear that inequities in the accessibility of quality treatment remain a primary challenge to improving health outcomes, and strategies that target specific barriers to quality healthcare are crucial to both eliminating current health disparities and preventing their further development.

Limitations of this study included the use of a large database such as the NCDB, which has been previously documented.45,46 The NCDB reports stage of disease at presentation, thus we are limited to patients who present with advanced disease. Surgeries performed on distant sites of disease have been underreported or miscoded, and the database only provides information on specific locations of distant metastases (the bone, brain, lungs, and liver). While staging for ovarian cancer specifies peritoneal metastasis beyond the pelvis, CRPM is defined by exclusion. This methodology is supported by the literature: Sherman et al isolated CRPM in the NCDB using this method, and Riihimaki et al identified the peritoneum as the most likely location following those already excluded.47,48 However, as cytoreductive surgery becomes more common across histologies, it would provide added clarification if the NCDB were to expand both the coding of surgery types and locations of metastatic disease to better facilitate detailed analyses. Additionally, the median zip code income, distance from hospital, and percent without a high school diploma are all based on census data aggregated to the patient’s zip code of residence, lacking specificity at the individual level. The patient population was also limited to individuals older than 40 years of age due to data availability. Additionally, reported race in electronic health records are often inconsistent when compared with self-reported race, with significant missingness and inaccuracies.49,50 Lastly, analyses of large databases like the NCDB can identify disparities but are unable to differentiate between systemic, cultural, or personal reasons for non-standard care, and studies targeted towards these relationships are necessary to fully understand the racial disparities in quality of care.

Cytoreductive surgery for CRPM was found to be associated with academic facilities, while cytoreductive surgery for ovarian cancer with peritoneal metastases was associated with a higher FIQ facility, private insurance, and patients listed as white. As complex surgeries become more common, it is likely that the gap in receipt of cytoreductive surgery will widen along socioeconomic and demographic disparities as CRPM becomes more amenable to surgical treatment, as it has historically with the introduction of new treatment modalities. In order to reduce current health disparities and prevent their further development as advanced treatment options continue to emerge, it is crucial to address the effects of systemic racism in healthcare and improve economic accessibility to quality care.

Supplementary Material

1720567_Sup_info

Synopsis:

Significant disparities exist in access to cytoreductive surgeries for patients with advanced ovarian cancer or colorectal cancer, with more sociodemographic and economic disparities prevailing among patients with ovarian cancer.

Funding/Support:

This research was supported by the University of Chicago Pritzker School of Medicine.

Role of Funder/Sponsor:

The funders of the study had no part in design and conduct of the study; collection, management, analysis, and interpretation of the data; preparation, review, or approval of the manuscript; and decision to submit the manuscript for publication.

Footnotes

Publisher's Disclaimer: This Author Accepted Manuscript is a PDF file of an unedited peer-reviewed manuscript that has been accepted for publication but has not been copyedited or corrected. The official version of record that is published in the journal is kept up to date and so may therefore differ from this version.

No disclosures to report.

Conflict of Interest Disclosures: There are no conflicts of interest.

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