Abstract
Background:
Centralization of rectal cancer surgery has been associated with high-quality oncologic care. However, several patient, disease and system-related factors can impact where patients receive care. We hypothesized that patients with low rectal tumors would undergo treatment at high-volume centers and would be more likely to receive guideline-based multidisciplinary treatment.
Methods:
Adults who underwent proctectomy for stage II/III rectal cancer were included from the Iowa Cancer Registry and supplemented with tumor location data. Multinomial logistic regression was employed to analyze factors associated with receiving care in high-volume hospital, while logistic regression for those associated with ≥12 lymph node yield, pre-operative chemoradiation and sphincter-preserving surgery.
Results:
Of 414 patients, 38%, 39%, and 22% had low, mid, and high rectal cancers, respectively. Thirty-two percent were >65 years, 38% female, and 68% had stage III tumors. Older age and rural residence, but not tumor location, were associated with surgical treatment in low-volume hospitals. Higher tumor location, high-volume, and NCI-designated hospitals had higher nodal yield (≥12). Hospital-volume was not associated with neoadjuvant chemoradiation rates or circumferential resection margin status. Sphincter-sparing surgery was independently associated with high tumor location, female sex, and stage III cancer, but not hospital volume.
Conclusions:
Low tumor location was not associated with care in high-volume hospitals. High-volume and NCI-designated hospitals had higher nodal yields, but not significantly higher neoadjuvant chemoradiation, negative circumferential margin, or sphincter preservation rates. Therefore, providing educational/quality improvement support in lower volume centers may be more pragmatic than attempting to centralize rectal cancer care among high-volume centers.
Keywords: Rectal cancer, Hospital volume, Rural surgery, Tumor location, Outcomes
Introduction
Current National Comprehensive Cancer Network (NCCN) guidelines for locally advanced rectal cancer (LARC) recommend the use of preoperative chemotherapy and radiation followed by an oncologic proctectomy.1 In the United States, the quality of this care pathway has been evaluated by standard metrics including the appropriate use of neoadjuvant chemoradiation, ≥12 lymph-node yield, and rates of sphincter-preservation and negative margins.2, 3 Historically, adherence to these guidelines has been variable across the country, resulting in worse outcomes when compliance was low.2, 4 Studies investigating the reasons for non-adherence to guideline-based treatments have identified several patient, disease, and system related variables, including age, socioeconomic factors, tumor distance from the anal verge, and surgeon/institution volume.5, 4, 6, 7
In a Surveillance, Epidemiology, and End Results (SEER)-Medicare data analysis, LARC patients who underwent surgical resection at National Cancer Institute (NCI) designated cancer centers or hospitals with residency programs or medical school affiliations were more likely to receive guideline concordant care.8 However, no difference in the proportion of patients undergoing sphincter-preserving surgery by facility type was observed. Similar findings were reported in another SEER patterns of care study, which analyzed a nationally representative sample of rectal cancer patients, showing that the receipt of guideline-recommended preoperative chemoradiation was significantly associated with treatment at larger hospitals (defined as >500 beds).9
Sphincter-preservation rates in the United States have been reported to vary between 48-77% and are impacted, besides tumor factors, by patient demographics, education, geography, and surgery center volume.10 While these factors have been studied individually in various populations, they have not been evaluated in the same cohort, making it challenging to discern whether the difference in quality of care is due to unmeasured case mix differences or actual variation in practice across institutions. For instance, tumors in the distal rectum are less likely to undergo sphincter-preservation but are thought to be more likely treated in high-volume institutions, while proximal tumors may not always need neoadjuvant treatment but have a greater likelihood of sphincter-preservation.
In this context, we sought to evaluate the association between patient demographics, tumor location, receipt of neoadjuvant chemoradiation, sphincter-sparing rates, and hospital-volume in the same state-wide patient cohort. We hypothesized that patients with low rectal tumors would be treated at high-volume hospitals, and that treatment at high-volume hospitals would be associated with increased rates of compliance to NCCN guidelines and sphincter-preserving approaches. Therefore, using Cancer Registry data from the rural state of Iowa (ICR), the current study aimed to: 1) determine demographic and clinicopathologic features, including rectal tumor location, associated with receiving care at high-volume hospitals; and 2) evaluate the association between hospital-volume and guideline recommended care including lymph node yield, pre-operative chemoradiation, and rates of sphincter-preserving surgery.
Patients & Methods
Patient Population
The ICR was queried for adults with microscopically confirmed stage II/III rectal cancer between 2013-2017 who received cancer-directed surgery. This is a population-based active surveillance registry and a member of the National Cancer Institute’s SEER program. It collects patient demographics, tumor characteristics, treatment data, and follow-up information on all cancers diagnosed or treated among residents of the state of Iowa.11 Distance from anal verge was coded as high, medium or low by a general surgery resident (GX) and ICR registrars. Because data on tumor height were collected as part of a study in which patients would be surveyed,12 inclusion criteria specified that patients had to be presumed to be alive as of October 2018. Exclusion criteria included having been diagnosed with another malignancy prior to rectal cancer, dying before receiving the survey, not receiving treatment with curative intent, wrong mailing address, and tumor abstraction after October 2018.
Study Variables
Patient demographics included age at diagnosis, sex, race/ethnicity, marital status at diagnosis, insurance, education, income, and rurality. Education, income, and rurality were categorized using residential Zone Improvement Program (ZIP) code. Education and income were extracted from the American Community Survey.13 Education was based on the percentage of individuals in the residential ZIP code with at least a bachelor’s degree split into quartiles (Quartile 1 (Q1): 0-27.5%, Q2-Q3: 27.8-38.1%, and Q4: 38.1-100%). Income was the average family income within the residential ZIP code. Utilizing the Rural-Urban Commuting Area (RUCA) 3-tier scheme developed at the University of Washington, rurality was classified into urban, large rural, and small rural.14 ICR data were employed to describe hospitals where patients underwent surgery. NCI designation was determined by the NCI Cancer Center online directory and included both NCI-designated Cancer hospitals and NCI-designated Comprehensive Cancer Centers.
Tumor characteristics included AJCC 7th edition stage, rectal tumor location, surgery type, receipt of radiation and chemotherapy as part of first course treatment. Patients undergoing low anterior resection (primary surgery site codes 30, 40) and abdominoperineal resection (codes 50, 70) were included. A hierarchy of available data to categorize tumor location was followed: 1) distance from anal verge (low: <6 cm, mid: 6-12 cm, high: >12-16 cm), 2) distance from dentate line, 3) distance from the anorectal ring, anal sphincter, or rectosigmoid junction, 4) location described as “low/distal”, “middle”, or “high/proximal”, 5) provider note of tumor being palpable on digital rectal exam (yes: low).
Data on proctectomies performed in Iowa hospitals were obtained from the Iowa Hospital Association (IHA) to investigate surgery volume. All discharge data records from the IHA with ICD-9 procedure codes 48.31 or 48.4-48.69, or ICD-10 codes 0DT.P0ZZ, 0DT.P4ZZ, 0DT.P7ZZ, 0DT.P8ZZ were included. The number of procedures each hospital performed were calculated. Patients who did not have a primary diagnosis of colorectal cancer or underwent local excision, destruction, or polypectomy surgeries were excluded. Surgical volume was categorized by the average number of proctectomies/year into low- (≤ 3), medium- (4-15), and high-volume (≥16) hospitals.12
Statistical analyses
In univariate analysis, Chi-square tests were for categorical variables and 2-sided t-tests were used for continuous variables. Variables with a cell count below 5 were omitted and replaced with a “*” per ICR privacy policies. Multinomial logistic regression was conducted comparing low- or medium- vs high-volume surgery hospitals. Additionally, logistic regression models were used to assess the following outcomes: nodal yield ≥12, neoadjuvant chemoradiation therapy, and sphincter-preserving low anterior resection (LAR) versus abdominoperineal resection (APR). This study was approved by the University of Iowa Institutional Review Board. Analyses were conducted in SAS version 9.4 (SAS Institute, Cary, NC).
Results
Of the 1,781 rectal cancers diagnosed between 2013 and 2017, 789 were microscopically confirmed stage II/III at the time of diagnosis and of those 664 received cancer directed surgery: 564 were first primaries. Among them, 61 patients did not meet inclusion criteria, while 89 (17.7%) died before the end of October 2018. Therefore, a total of 414 patients were included: 32% were >65 years, 38% were female, and 4% non-white. Over 50% were living in rural areas. Tumor location was categorized as low in 39% of cases, mid in 38%, and high in 22%. Overall, 32% were stage II, and 68% stage III. Seventy percent of the patients underwent a LAR and 30% an APR, with 14% of the proctectomies performed at low-, 21% at medium-, and 65% at high-volume hospitals.
Cohort by Tumor location
The distribution of age, sex, race, marital status, insurance status, income, education, rurality, and stage did not differ by tumor location (Table 1). Sphincter-sparing surgery was more commonly performed for higher tumor locations, with 36% of low, 86% of mid, and 98% of high tumors undergoing a LAR as opposed to an APR (p<0.001). Similarly, there was an increased rate of nodal yield ≥12 in those patients with high tumor location (p=0.003), while neoadjuvant chemoradiation was more frequently administered to individuals with low rectal tumors (low=80%, mid=78%, high=47%, p=0.001).
Table 1.
Association between clinicopathologic characteristics and tumor location in patients with stage II/III rectal cancers who underwent resection.
| Characteristics | Tumor Location | p-value | ||
|---|---|---|---|---|
|
Low N=162 (%) |
Mid N=160 (%) |
High N=92 (%) |
||
| Total | ||||
| Age >65 years old | 55 (34.0) | 44 (27.5) | 33 (35.9) | 0.300 |
| Female Sex | 54 (33.3) | 71 (44.4) | 31 (33.7) | 0.083 |
| Non-white Race | 5 (3.1) | 5 (3.1) | 5 (5.4) | 0.574 |
| Married | 104 (64.2) | 104 (65.0) | 68 (73.9) | 0.244 |
| Public Insurance | 90 (55.6) | 76 (47.5) | 45 (48.9) | 0.318 |
| Rurality | 0.421 | |||
| Small rural | 60 (37.0) | 68 (42.5) | 29 (31.5) | |
| Large rural | 24 (14.8) | 18 (11.3) | 16 (17.4) | |
| Urban | 78 (48.2) | 74 (46.3) | 47 (51.1) | |
| Income | 0.366 | |||
| $35000 to 50000 | 46 (28.6) | 49 (30.8) | 22 (24.2) | |
| $50001 to 75000 | 101 (62.7) | 92 (57.9) | 54 (59.3) | |
| >$75000 | 14 (8.7) | 18 (11.3) | 15 (16.5) | |
| Bachelor’s Degree | 0.436 | |||
| <1st quartile | 42 (25.9) | 39 (24.4) | 19 (20.9) | |
| 1st-3rd quartile | 75 (46.3) | 88 (55.0) | 47 (51.7) | |
| >3rd quartile | 45 (27.8) | 33 (20.6) | 25 (27.5) | |
| Nodal stage | 0.125 | |||
| N0 | 43 (2.6.5) | 50 (31.3) | 38 (41.3) | |
| N1 | 90 (55.6) | 87 (54.4) | 45 (48.9) | |
| N2 | 29 (17.9) | 23 (14.4) | 9 (9.8) | |
| Overall Stage | 0.052 | |||
| II | 43 (26.5) | 50 (31.3) | 38 (41.3) | |
| III | 119 (73.5) | 110 (68.8) | 54 (58.7) | |
| Nodal Yield ≥12 | 127 (78.4) | 117 (73.1) | 84 (91.3) | 0.003 |
| Surgical Volume | 0.491 | |||
| Low | 16 (10.5) | 22 (14.3) | 16 (17.8) | |
| Medium | 35 (22.9) | 32 (20.8) | 15 (16.7) | |
| High | 102 (66.7) | 100 (64.9) | 59 (65.6) | |
| Surgery | <.001 | |||
| Abdominoperineal Resection | 100 (64.5) | 22 (13.8) | * | |
| Low Anterior Resection | 62 (35.5) | 138 (86.2) | 90 (97.8) | |
| National Cancer Institute designated | 44 (28.6) | 40 (26.0) | 16 (17.6) | 0.150 |
| Preoperative chemoradiation | 129 (79.6) | 124 (77.5) | 43 (46.7) | 0.001 |
Bolded p-values meet statistical significance (p <.05). Variables with cell counts below 5 were omitted and replaced with a “*” per Iowa Cancer Registry privacy policies.
Hospital Surgical Volume
In univariate analysis, patients >65 years, those residing in small rural areas, and with median household income of <$50,000 were more likely to undergo surgery at low-volume hospitals (Table 2). There were no differences in gender, race, marital and insurance status, overall stage, tumor location, sphincter-preserving surgery, and neoadjuvant chemoradiation rates among the three hospital-volume groups. A lower proportion of patients had nodal yield ≥12 at low-volume hospitals as compared to medium- and high-volume facilities (p=0.001).
Table 2.
Association between clinicopathologic characteristics and hospital surgical volume for patients with stage II/III rectal cancers who underwent resection.
| Characteristics | Surgical Volume | p-value | ||
|---|---|---|---|---|
|
Low
N=55 (%) |
Medium
N=84 (%) |
High
N=261 (%) |
||
| Total | ||||
| Age >65 years old | 27 (49.1) | 26 (31.0) | 73 (28.0) | 0.009 |
| Female Sex | 24 (43.6) | 28 (33.3) | 97 (37.2) | 0.47 |
| Non-white Race | * | * | 11 (4.2) | 0.346 |
| Married | 39 (70.9) | 52 (61.9) | 176 (67.4) | 0.504 |
| Public Insurance | 33 (60.0) | 47 (56.0) | 122 (46.7) | 0.108 |
| Rurality | 0.017 | |||
| Small rural | 29 (52.7) | 29 (34.5) | 92 (35.3) | |
| Large rural | 11 (20.0) | 9 (10.7) | 37 (14.2) | |
| Urban | 15 (27.3) | 46 (54.8) | 132 (50.6) | |
| Income | 0.001 | |||
| $35000-50000 | 26 (48.2) | 19 (22.6) | 68 (26.2) | |
| $50001-75000 | 27 (50.0) | 58 (69.1) | 152 (58.5) | |
| >$75000 | * | 7 (8.3) | 40 (15.4) | |
| Bachelor’s Degree | 0.004 | |||
| <1st quartile | 15 (27.3) | 18 (21.4) | 62 (23.9) | |
| 1st-3rd quartile | 37 (62.3) | 46 (54.8) | 120 (46.2) | |
| >3rd quartile | 3 (5.5) | 20 (23.8) | 78 (30.0) | |
| Nodal Stage | 0.113 | |||
| N0 | 22 (40.0) | 19 (22.6) | 86 (33.0) | |
| N1 | 27 (49.1) | 47 (56.0) | 141 (54.0) | |
| N2 | 6 (10.9) | 18 (21.4) | 34 (13.0) | |
| Overall Stage | 0.077 | |||
| II | 22 (40.0) | 19 (22.6) | 86 (33.0) | |
| III | 33 (60.0) | 65 (77.4) | 175 (67.1) | |
| Surgery Group | 0.175 | |||
| Abdominoperineal resection | 11 (20.0) | 29 (34.5) | 80 (30.7) | |
| Low anterior resection | 44 (80.0) | 55 (65.5) | 181 (69.3) | |
| Nodal Yield ≥12 | 34 (61.8) | 70 (83.3) | 216 (82.8) | 0.001 |
| Tumor Location | 0.491 | |||
| Low | 16 (29.6) | 35 (42.7) | 102 (39.1) | |
| Mid | 22 (40.7) | 32 (39.0) | 100 (38.3) | |
| High | 16 (29.6) | 15 (18.3) | 59 (22.6) | |
| Preoperative chemoradiation | 36 (65.5) | 57 (67.9) | 192 (73.6) | 0.358 |
Bold p-values meet statistical significance (p < .05). Variables with cell counts below 5 were omitted and replaced with a “*” per Iowa Cancer Registry privacy policies.
In multinomial logistic regression comparing patients who received surgery at low- and medium-volume hospitals versus high-volume hospitals, older age and living in small rural areas remained associated with increased odds of having surgery at a low-volume hospitals (OR= 2.5, 95% confidence interval [CI] 1.3-4.7, and OR= 2.6, CI 1.2-5.4, respectively; Table 3). Tumor location and stage were not significantly associated with hospital-volume.
Table 3.
Multinomial logistic regression analysis comparing clinicopathologic characteristics and hospital surgical volume for patients with stage II/III rectal cancers who underwent resection.
| Variable | Hospital Surgical Volume | Odds Ratio | 95% Confidence Interval | P-value | ||
|---|---|---|---|---|---|---|
| Lower bound | Upper bound | |||||
| Age | > 65 years vs ≤ 65 years | low | 2.45 | 1.29 | 4.65 | 0.006 |
| > 65 years vs ≤ 65 years | medium | 1.26 | 0.73 | 2.19 | 0.411 | |
| Rurality | Large rural vs Urban | low | 2.61 | 1.04 | 6.58 | 0.041 |
| Large rural vs Urban | medium | 0.73 | 0.33 | 1.64 | 0.445 | |
| Small rural vs Urban | low | 2.59 | 1.24 | 5.39 | 0.011 | |
| Small rural vs urban | medium | 0.90 | 0.51 | 1.55 | 0.684 | |
| Tumor location | Medium vs Low | low | 1.79 | 0.83 | 3.87 | 0.140 |
| Medium vs Low | medium | 0.95 | 0.54 | 1.66 | 0.852 | |
| High vs Low | low | 2.07 | 0.89 | 4.82 | 0.093 | |
| High vs Low | medium | 0.78 | 0.39 | 1.56 | 0.482 | |
| Tumor stage | III vs II | low | 0.78 | 0.41 | 1.50 | 0.460 |
| III vs II | medium | 1.73 | 0.96 | 3.12 | 0.069 | |
Bold p-values meet statical significance (p <.05).
High-volume hospital was the reference group.
Neoadjuvant Chemoradiation therapy
In univariate analysis, older individuals (>65 years) received chemoradiation therapy less often than younger patients (29% vs 39%, p=0.043; analyses not shown). No differences were observed in rates of neoadjuvant therapy based on gender, race, marital and insurance status, rurality, income, education, or tumor stage. However, neoadjuvant chemoradiation was more often administered to patients with low tumors (low =44%, mid=42%, high=15%, p=0.001), and was associated with significantly lower rates of nodal yield ≥12 (76% vs 87%, p=0.012).
On multivariable analysis, demographic characteristics and hospital-volume were not associated with receipt of neoadjuvant chemoradiation (Table 4). Patients living in small rural areas were less likely to receive neoadjuvant chemoradiation compared to individuals in urban areas (OR= 0.5, CI 0.3-0.8), but no difference was found between large rural and urban areas. High tumor location was associated with lower odds of undergoing neoadjuvant chemoradiation compared to low tumors (OR= 0.2, CI 0.1-0.4).
Table 4.
Multivariable analysis comparing clinicopathologic characteristics and receipt of chemoradiation for patients with stage II/III rectal cancers who underwent resection.
| Variables | Odds Ratio | 95% confidence interval | P-Value | ||
|---|---|---|---|---|---|
| Lower Bound | Upper Bound | ||||
| Rectal volume | Low vs High | 0.74 | 0.35 | 1.56 | 0.429 |
| Medium vs High | 0.65 | 0.37 | 1.16 | 0.142 | |
| Tumor location | Mid vs Low | 0.79 | 0.44 | 1.39 | 0.409 |
| High vs Low | 0.19 | 0.10 | 0.35 | <.001 | |
| Age | > 65 years vs ≤ 65 years | 0.67 | 0.40 | 1.11 | 0.116 |
| Nodal Yield | ≥12 vs <12 | 2.00 | 1.02 | 3.93 | 0.043 |
| Marital status | Married vs Unmarried | 1.45 | 0.87 | 2.41 | 0.158 |
| Rurality | Large rural vs Urban | 0.84 | .40 | 1.77 | 0.652 |
| Small rural vs Urban | 0.49 | 0.29 | 0.84 | 0.010 | |
Bold p-values meet statistical significance (p <.05).
Surgical approach
Females were more likely to undergo LAR rather than APR (42% vs 27%, p=0.001; analyses not shown). Surgical approach did not differ by age, race, marital or insurance status, rurality, income, and education level. Additionally, there was a similar distribution of nodal status, overall stage, and lymph node yield between the two groups. Patients with lower tumors were more likely to undergo an APR (65%) than LAR (36%, p=0.001) and to receive neoadjuvant chemoradiation (p=0.005). Among patients with available data on circumferential resection margin (CRM; 74%), 6% (n=18) were positive. There was no difference based on hospital-volume (p=0.06), although CRM involvement increased with proximity to the anal verge in all low, mid, and high-volume institutions (data not shown per registry policy).
In multivariate analysis, compared to APR, males had lower odds of receiving a LAR (OR= 0.5, CI 0.3-0.8; Table 5). Conversely, patients with mid and high tumors were more likely to have a LAR than those with low tumors (mid: OR= 13.3, CI 7.3-24.5; high: OR= 111.8, CI 25.5-489.9). Hospital-volume was not associated with differences in surgical approach.
Table 5.
Multivariable analysis comparing clinicopathologic characteristics and odds of undergoing low anterior resection for patients with stage II/III rectal cancers who underwent resection.
| Effect | Odds Ratio | 95% confidence interval | P-Value | ||
|---|---|---|---|---|---|
| Lower Bound | Upper Bound | ||||
| Rectal volume | Low vs High | 0.99 | 0.39 | 2.54 | 0.989 |
| Medium vs High | 0.85 | 0.43 | 1.69 | 0.645 | |
| Tumor location | Mid vs Low | 13.34 | 7.26 | 24.54 | <.001 |
| High vs Low | 111.78 | 25.51 | 489.88 | <.001 | |
| Sex | Male vs Female | 0.46 | 0.26 | 0.84 | 0.010 |
| Stage | III vs II | 1.98 | 1.06 | 3.67 | 0.031 |
| Income | $35000-50000 vs >$75000 | 2.29 | 0.84 | 6.2 | 0.104 |
| $50000-75000 vs >$75000 | 2.33 | 0.93 | 5.85 | 0.071 | |
Bold p-values meet statistical significance (p< .05).
Nodal Yield
In unadjusted analyses, nodal yield ≥12 was significantly associated with older age, living in an urban area, higher income levels, higher education, and high tumor location, but not with gender, race, marital status, insurance status, overall stage, and surgical approach.
After adjustment for available confounders, older age, higher income, high tumor location, and lack of neoadjuvant chemoradiation were found to be significantly associated with a nodal yield ≥12. Additionally, patients undergoing surgery at low-volume hospitals had lower odds of a nodal yield ≥12 compared to mid- and high-volume hospitals (OR= 0.4, CI 0.2-0.8; Table 6).
Table 6.
Multivariable analysis comparing clinicopathologic characteristics and nodal yield ≥12 for patients with stage II/III rectal cancers who underwent resection.
| Effect | Odds Ratio | 95% confidence Interval | P-value | ||
|---|---|---|---|---|---|
| Lower Bound | Upper Bound | ||||
| Tumor location | Mid vs Low | 0.71 | 0.40 | 1.26 | 0.24 |
| High vs Low | 2.75 | 1.09 | 6.97 | 0.033 | |
| Age | > 65 years vs ≤ 65 years | 0.51 | 0.29 | 0.89 | 0.017 |
| Preoperative chemoradiation | Received vs Not received | 0.51 | 0.26 | 0.99 | 0.048 |
| Rectal volume | Low vs High | 0.40 | 0.20 | 0.84 | 0.015 |
| Medium vs High | 1.11 | 0.56 | 2.21 | 0.766 | |
| Income | $35000-50000 vs >$7500 | 0.14 | 0.03 | 0.62 | 0.01 |
| $50000-75000 vs >$75000 | 0.25 | 0.06 | 1.08 | 0.063 | |
Bold p-values meet statistical significance (p< .05).
Discussion
In this population-based cohort of patients from a rural state with locally advanced rectal cancer, we observed that younger individuals and those living in urban settings were more likely to undergo treatment at high-volume hospitals, while location of the tumor did not impact where patients received surgical care. Patients who underwent surgical resection at low-volume hospitals compared to mid- and high-volume hospitals were less likely to have a nodal yield of ≥12. However, treatment at high-volume institutions was not associated with higher rates of receiving neoadjuvant chemoradiation, negative CRM, or sphincter-preserving surgeries.
Following the individual diagnosis of rectal cancer in a patient, the subsequent setting where they receive care is influenced by the diagnosing endoscopist, the referring providers, and the multidisciplinary team that eventually treats the patient. These dynamics are further impacted by patient preferences and characteristics, as well as the patients’ healthcare system. In our cohort, older age and living in a rural area were associated with receiving care at low-volume hospitals. These findings are consistent with the findings of Chioreso et al., who found that among older patients with stage II/III rectal adenocarcinoma (n=1,601) those living in rural communities were less likely to seek care at high-volume hospitals.15 Among the disease specific factors that can affect where patients undergo treatment is the location of the tumor, as distal or low rectal cancers are more likely to require an APR, considered to require greater technical expertise and more likely to be performed in high-volume hospitals. However, our data suggests that rectal tumor location does not significantly impact where patients with LARC receive surgical care. These findings, along with observations from other studies, suggest that certain subsets of patients may have practical issues like transportation and/or prefer the familiarity with their local hospital.16 As a result, these factors may be more influential in where they receive care rather than the specific features of their cancer or the knowledge of the quality of care in high-volume centers.16 This contention is supported by findings from a consumer survey of 2,004 random adults throughout the United States that found that the most influential factors in the decision making of where to receive care were hospital reputation (62%) and primary care physician opinion (53%).17 While hospital-volume was an important factor for 37% of the cohort, just above risk of death (35%); guidelines adherent care was relevant for only 18% of the patients.
Several reports have demonstrated that patients being treated at high-volume hospitals are more likely to receive guideline concordant care and have better outcomes.18, 19 Del Paggio et al. in an Ontario population-based cohort study showed that hospital-volume was associated with a significantly higher nodal yield amongst colorectal cancer patients.20 Our analyses also found that high-volume hospitals were more likely to remove/examine ≥12 lymph nodes and corresponds to findings from previous studies supporting the relationship between high-volume and achievement of such performance metrics for rectal cancer.2, 21 It is also necessary to consider the fact that in our study this difference in lymph node yield was only between low-volume hospitals (<3 cases/year ) compared to mid- (4-15) and high (>16) volume hospitals, while it was similar between the mid and high-volume hospitals. In fact, the perceived adverse impact of receiving care in low-volume hospitals compared to high-volume hospital has not been consistently demonstrated in the literature.22, 23 A significant consideration in the studies evaluating this relationship has been the volume cut-offs that were used and if they are clinically relevant. It is likely that some of the variations in the associations between oncologic outcomes and surgical volumes are in part due to difference in case definitions and study methodology rather than variations in actual care delivery. Furthermore, the yield of lymph nodes can be independently impacted by neoadjuvant treatment, as shown with our analyses, and is also a function of the pathologists who examine the specimen and not just the quality of the surgery.24
In contrast to our hypothesis, hospital-volume did not correlate with other quality metrics, such as rates of sphincter-preservation, CRM involvement, or receipt of neoadjuvant chemoradiation. The association between hospital-volume and sphincter-preservation rates in previous reports has been inconsistent and confounded by the fact that tumor location was not always accounted for in the analysis. While low tumors are more likely to require an APR due to oncologic considerations, high APR rates can be due to the lack of expertise in sphincter-preservation. We did not observe an association between hospital-volume and rates of sphincter-preservation after adjustment for patient and disease characteristics including tumor location. Similarly, in a retrospective study of 1,469 patients with rectal adenocarcinoma, Leonard et al. found that high-volume hospitals were not significantly associated with higher rates of sphincter-preservation.25 Conversely, in a 2004 nested cohort study of 1,330 patients with LARC, Meyerhardt et al. reported a significantly increased rate of APR at low-volume hospitals compared to larger institutions (46% vs 32%, p<0.001), regardless of tumor distance from the anal verge.26 This study differed methodologically from ours in that it was conducted on patients enrolled in a neoadjuvant treatment trial. Therefore, these patients were under strict treatment protocols and may not have experienced therapeutic variations between high- and low-volume hospitals as would normally be seen.
Finally, our study found that while neoadjuvant chemoradiation rates varied by tumor location, consistent with current practice guidelines, it was not associated with hospital-volume.27, 1 These findings stand in contrast to those by Gan et al., who in a cohort of 1,896 patients with LARC, found that treatment at large academic centers was associated with higher likelihood of receiving neoadjuvant therapy, although tumor location was not available to the investigators.28
Centralization of cancer care has been advocated as a means of improving quality of care and oncologic outcomes in rectal cancer.2, 29, 30 The rationale stems from data demonstrating improved adherence to performance and quality measures at high-volume hospitals.5, 31 Our data demonstrate that low- and medium-volume hospitals in rural Iowa are able to achieve important performance measures, including neoadjuvant chemoradiation, CRM clearance, and sphincter-preservation, at rates comparable to high-volume hospitals. The relevance of these observations are contextualized by the fact that low- and mid-volume hospitals often serve a greater proportion of patients who are older, Black and Hispanic, Medicare and/or Medicaid, and who do not want to travel far for care.32, 33 As such, centralization or regionalization of health care to high-volume hospitals has the potential to worsen healthcare inequalities, decrease access to care in rural areas, and exacerbate workload at potentially overburdened high-volume hospitals.34–37
The limitations of this retrospective cohort study include the inability to directly evaluate causality between measured outcomes and study variables. This cohort is derived from a secondary analysis of a 2018 survey study of rectal cancer patients; therefore, only those who survived and were able to complete the questionnaire were included. Because of the unknown number of patients who died before the survey was administered, there is a significant potential for selection bias which could impact current findings. Therefore, these data should be interpreted in the context of this limitation. Due to lack of granularity, certain confounders may not be adjusted for, such as chemoradiation regimens, grade of mesorectal specimen, rate of complete pathologic response, or individual surgeon volume and specialty. Presenting patient symptoms such as obstruction or perforation which may determine whether a patient receives upfront surgical intervention instead of neoadjuvant chemoradiation are not recorded in the database. Moreover, survival and recurrence data were also not available; however, the focus of this study was short-term oncologic outcomes and care patterns. This study also focused on a rural, Midwestern state with a largely homogenous population, which limits its generalizability to the United States population.
In conclusion, in this state-wide cohort of LARCs, while older patients and those living in rural areas were less likely to receive care at a high-volume hospital, tumor location did not impact patterns of care, suggesting that the decision of where to receive multidisciplinary rectal cancer care might be mainly driven by geographic convenience. Although medium and high-volume hospitals were more often associated with nodal yield ≥12, they did not have higher neoadjuvant chemoradiation, negative CRM, or sphincter-preservation rates. Our results suggest that centralization of care should be based on pragmatic and practical considerations, and that providing educational and quality improvement support focused on nodal yield would be beneficial for health care providers practicing in low-volume centers.
Acknowledgments
This research was supported by NIH/NCI contract number HHSN261201800012I/HHSN26100001 (MEC, ARK); NIH/NCI K07 Cancer Prevention, Control, Behavioral Sciences and Population Sciences Career Development Award: 1K07CA197067 (MEC, NJD); NIH grant T32 CA 148062 (XG), and NIH/NCI P30 CA086862 (MEC, ARK).
Footnotes
Disclosure: The authors have nothing to disclose.
References
- 1.NCCN. NCCN Clinical Practice Guidelines in Oncology: Rectal Cancer. https://www.nccn.org/professionals/physician_gls/pdf/rectal.pdf. 2021. Accessed January 2021 2021.
- 2.Brady JT, Xu Z, Scarberry KB, Saad A, Fleming FJ, Remzi FH et al. Evaluating the Current Status of Rectal Cancer Care in the US: Where We Stand at the Start of the Commission on Cancer’s National Accreditation Program for Rectal Cancer. J Am Coll Surg. 2018;226(5):881–90. doi: 10.1016/j.jamcollsurg.2018.01.057. [DOI] [PubMed] [Google Scholar]
- 3.Shulman LN, Browner AE, Palis BE, Mallin K, Kakade S, Carp N et al. Compliance with Cancer Quality Measures Over Time and Their Association with Survival Outcomes: The Commission on Cancer’s Experience with the Quality Measure Requiring at Least 12 Regional Lymph Nodes to be Removed and Analyzed with Colon Cancer Resections. Annals of surgical oncology. 2019;26(6):1613–21. doi: 10.1245/s10434-019-07323-w. [DOI] [PubMed] [Google Scholar]
- 4.Lee L, Dietz DW, Fleming FJ, Remzi FH, Wexner SD, Winchester D et al. Accreditation Readiness in US Multidisciplinary Rectal Cancer Care: A Survey of OSTRICH Member Institutions. JAMA Surg. 2018;153(4):388–90. doi: 10.1001/jamasurg.2017.4871. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 5.Monson JR, Probst CP, Wexner SD, Remzi FH, Fleshman JW, Garcia-Aguilar J et al. Failure of evidence-based cancer care in the United States: the association between rectal cancer treatment, cancer center volume, and geography. Ann Surg. 2014;260(4):625–31; discussion 31-2. doi: 10.1097/sla.0000000000000928. [DOI] [PubMed] [Google Scholar]
- 6.Koëter T, de Nes LCF, Wasowicz DK, Zimmerman DDE, Verhoeven RHA, Elferink MA et al. Hospital variation in sphincter-preservation rates in rectal cancer treatment: results of a population-based study in the Netherlands. BJS Open. 2021;5(4). doi: 10.1093/bjsopen/zrab065. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 7.Paquette IM, Kemp JA, Finlayson SR. Patient and hospital factors associated with use of sphincter-sparing surgery for rectal cancer. Dis Colon Rectum. 2010;53(2):115–20. doi: 10.1007/DCR.0b013e3181bc98a1. [DOI] [PubMed] [Google Scholar]
- 8.Charlton ME, Hrabe JE, Wright KB, Schlichting JA, McDowell BD, Halfdanarson TR et al. Hospital Characteristics Associated with Stage II/III Rectal Cancer Guideline Concordant Care: Analysis of Surveillance, Epidemiology and End Results-Medicare Data. J Gastrointest Surg. 2016;20(5):1002–11. doi: 10.1007/s11605-015-3046-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 9.Del Vecchio NJ, Schlichting JA, Chioreso C, Kahl AR, Hrabe JE, Lynch CF et al. Guideline-Recommended Chemoradiation for Patients With Rectal Cancer at Large Hospitals: A Trend in the Right Direction. Diseases of the colon and rectum. 2019;62(10):1186–94. doi: 10.1097/dcr.0000000000001452. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 10.Temple LK, Romanus D, Niland J, Veer AT, Weiser MR, Skibber J et al. Factors associated with sphincter-preserving surgery for rectal cancer at national comprehensive cancer network centers. Ann Surg. 2009;250(2):260–7. doi: 10.1097/SLA.0b013e3181ae330e. [DOI] [PubMed] [Google Scholar]
- 11.National Cancer Institute. Surveillance, Epidemiology, and End Results Program. 2018. [Google Scholar]
- 12.Del Vecchio N, Gao X, Weeks K, Mengeling M, Kahl A, Gribovskaja-Rupp I et al. Referrals and deciscion-making considerations involved in selecting a surgeon for rectal cancer treatent. Disceases of the Colon and Rectum. 2021; 10.1097/DCR.0000000000002257. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 13.Bureau.; USC. 2013-2017 American Community Servey Public Use Microdata Samples. 2021.
- 14.Washington Uo. Rural-Urban Community Area Codes (RUCAs). Rural Health Research Center. 2005. http://depts.washington.edu/uwruca/. Accessed May 22 2019. [Google Scholar]
- 15.Chioreso C, Gao X, Gribovskaja-Rupp I, Lin C, Ward MM, Schroeder MC et al. Hospital and Surgeon Selection for Medicare Beneficiaries With Stage II/III Rectal Cancer: The Role of Rurality, Distance to Care, and Colonoscopy Provider. Ann Surg. 2019. doi: 10.1097/sla.0000000000003673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 16.Fong ZV, Lim PW, Hendrix R, Castillo CF, Nipp RD, Lindberg JM et al. Patient and Caregiver Considerations and Priorities When Selecting Hospitals for Complex Cancer Care. Annals of surgical oncology. 2021;28(8):4183–92. doi: 10.1245/s10434-020-09506-2. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 17.Ellis RJ, Yuce TK, Hewitt DB, Merkow RP, Kinnier CV, Johnson JK et al. National Evaluation of Patient Preferences in Selecting Hospitals and Health Care Providers. Medical care. 2020;58(10):867–73. doi: 10.1097/mlr.0000000000001374. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 18.Aquina CT, Probst CP, Becerra AZ, Iannuzzi JC, Kelly KN, Hensley BJ et al. High volume improves outcomes: The argument for centralization of rectal cancer surgery. Surgery. 2016;159(3):736–48. doi: 10.1016/j.surg.2015.09.021. [DOI] [PubMed] [Google Scholar]
- 19.Huo YR, Phan K, Morris DL, Liauw W. Systematic review and a meta-analysis of hospital and surgeon volume/outcome relationships in colorectal cancer surgery. Journal of gastrointestinal oncology. 2017;8(3):534–46. doi: 10.21037/jgo.2017.01.25. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 20.Del Paggio JC, Nanji S, Wei X, MacDonald PH, Booth CM. Lymph node evaluation for colon cancer in routine clinical practice: a population-based study. Curr Oncol. 2017;24(1):e35–e43. doi: 10.3747/co.24.3210. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 21.Rhoads KF, Ackerson LK, Ngo JV, Gray-Hazard FK, Subramanian SV, Dudley RA. Adequacy of lymph node examination in colorectal surgery: contribution of the hospital versus the surgeon. Med Care. 2013;51(12):1055–62. doi: 10.1097/MLR.0b013e3182a53d72. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 22.Salz T, Sandler RS. The effect of hospital and surgeon volume on outcomes for rectal cancer surgery. Clinical gastroenterology and hepatology : the official clinical practice journal of the American Gastroenterological Association. 2008;6(11):1185–93. doi: 10.1016/j.cgh.2008.05.023. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 23.Link KH, Coy P, Roitman M, Link C, Kornmann M, Staib L. Minimum Volume Discussion in the Treatment of Colon and Rectal Cancer: A Review of the Current Status and Relevance of Surgeon and Hospital Volume regarding Result Quality and the Impact on Health Economics. Visceral Medicine. 2017;33(2):140–7. doi: 10.1159/000456044. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 24.Abdel-Misih SR, Wei L, Benson AB 3rd, Cohen S, Lai L, Skibber J et al. Neoadjuvant Therapy for Rectal Cancer Affects Lymph Node Yield and Status Without Clear Implications on Outcome: The Case for Eliminating a Metric and Using Preoperative Staging to Guide Therapy. Journal of the National Comprehensive Cancer Network : JNCCN. 2016;14(12):1528–34. doi: 10.6004/jnccn.2016.0164. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 25.Leonard D, Penninckx F, Kartheuser A, Laenen A, Van Eycken E. Effect of hospital volume on quality of care and outcome after rectal cancer surgery. Br J Surg. 2014;101(11):1475–82. doi: 10.1002/bjs.9624. [DOI] [PubMed] [Google Scholar]
- 26.Meyerhardt JA, Tepper JE, Niedzwiecki D, Hollis DR, Schrag D, Ayanian JZ et al. Impact of hospital procedure volume on surgical operation and long-term outcomes in high-risk curatively resected rectal cancer: findings from the Intergroup 0114 Study. J Clin Oncol. 2004;22(1):166–74. doi: 10.1200/jco.2004.04.172. [DOI] [PubMed] [Google Scholar]
- 27.Glynne-Jones R, Wyrwicz L, Tiret E, Brown G, Rödel C, Cervantes A et al. Rectal cancer: ESMO Clinical Practice Guidelines for diagnosis, treatment and follow-up. Ann Oncol. 2018;29(Suppl 4):iv263. doi: 10.1093/annonc/mdy161. [DOI] [PubMed] [Google Scholar]
- 28.Gan T, Chen Q, Huerta CT, Huang B, Evers BM, Patel JA. Neoadjuvant Therapy in Stage II/III Rectal Cancer: A Retrospective Study in a Disparate Population and the Effect on Survival. Dis Colon Rectum. 2021;64(10):1212–21. doi: 10.1097/dcr.0000000000001977. [DOI] [PubMed] [Google Scholar]
- 29.Wexner SD, Berho ME. The Rationale for and Reality of the New National Accreditation Program for Rectal Cancer. Dis Colon Rectum. 2017;60(6):595–602. doi: 10.1097/dcr.0000000000000840. [DOI] [PubMed] [Google Scholar]
- 30.Hosseinali Khani M, Smedh K. Centralization of rectal cancer surgery improves long-term survival. Colorectal Disease. 2010;12(9):874–9. [DOI] [PubMed] [Google Scholar]
- 31.Hodgson DC, Zhang W, Zaslavsky AM, Fuchs CS, Wright WE, Ayanian JZ. Relation of hospital volume to colostomy rates and survival for patients with rectal cancer. Journal of the National Cancer Institute. 2003;95(10):708–16. [DOI] [PubMed] [Google Scholar]
- 32.Xu Z, Becerra AZ, Justiniano CF, Boodry CI, Aquina CT, Swanger AA et al. Is the Distance Worth It? Patients With Rectal Cancer Traveling to High-Volume Centers Experience Improved Outcomes. Dis Colon Rectum. 2017;60(12):1250–9. doi: 10.1097/dcr.0000000000000924. [DOI] [PubMed] [Google Scholar]
- 33.Dimick J, Ruhter J, Sarrazin MV, Birkmeyer JD. Black patients more likely than whites to undergo surgery at low-quality hospitals in segregated regions. Health Aff (Millwood). 2013;32(6):1046–53. doi: 10.1377/hlthaff.2011.1365. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 34.Stitzenberg KB, Sigurdson ER, Egleston BL, Starkey RB, Meropol NJ. Centralization of cancer surgery: implications for patient access to optimal care. J Clin Oncol. 2009;27(28):4671–8. doi: 10.1200/jco.2008.20.1715. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 35.Huguet M. Centralization of care in high volume hospitals and inequalities in access to care. Soc Sci Med. 2020;260:113177. doi: 10.1016/j.socscimed.2020.113177. [DOI] [PubMed] [Google Scholar]
- 36.Sheetz KH, Dimick JB, Nathan H. Centralization of High-Risk Cancer Surgery Within Existing Hospital Systems. Journal of Clinical Oncology. 2019;37(34):3234–42. doi: 10.1200/jco.18.02035. [DOI] [PMC free article] [PubMed] [Google Scholar]
- 37.Schlottmann F, Charles AG, Patti MG. Challenges of centralizing cancer care in the US. Int J Surg. 2018;55:209–10. doi: 10.1016/j.ijsu.2018.05.002. [DOI] [PubMed] [Google Scholar]