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© 2003 American Society for Clinical Oncology Use of Adjuvant Chemotherapy and Radiation Therapy for Colorectal Cancer in a Population-Based Cohort
From the Division of General Medicine and Channing Laboratory, Department of Medicine, Brigham and Women’s Hospital and Harvard Medical School; Department of Health Care Policy, Harvard Medical School; and Division of Medical Oncology, Dana-Farber Cancer Institute, Boston, MA; Cancer Surveillance Program and Cancer Surveillance Section, California Department of Health Services, Sacramento; Public Health Institute, Berkeley; and Northern California Cancer Center, Union City, CA. Address reprint requests to John Z. Ayanian, MD, MPP, Department of Health Care Policy, Harvard Medical School, 180 Longwood Ave, Boston, MA 02115; email: ayanian{at}hcp.med.harvard.edu.
Purpose: Randomized trials have demonstrated that adjuvant chemotherapy improves survival for patients with stage III colon cancer and that chemotherapy combined with radiation therapy improves survival for patients with stage II or III rectal cancer. This population-based study was designed to assess use of these treatments in clinical practice. Patients and Methods: From the California Cancer Registry, we identified all patients diagnosed during 1996 to 1997 with stage III colon cancer (n = 1,422) and stage II or III rectal cancer (n = 534) in 22 northern California counties. To supplement registry data on adjuvant therapies and ascertain reasons they were not used, we surveyed physicians or reviewed office records for 1,449 patients (74%).
Results: Chemotherapy rates varied widely by age from 88% (age < 55 years) to 11% (age Conclusion: Use of adjuvant therapy for colorectal cancer varies substantially by age, race, marital status, hospital volume, and individual hospital, indicating opportunities to improve care. With enhanced data on adjuvant therapies, population-based registries could become a valuable resource for monitoring the quality of cancer care.
COLORECTAL CANCER is diagnosed in approximately 135,000 people annually in the United States, and 57,000 people die from this disease, making it the second most common malignant cause of death in this country.1 Randomized clinical trials have demonstrated that adjuvant chemotherapy improves survival for patients with stage III colon cancer.2–6 For patients with stage II or III rectal cancer, the combination of adjuvant chemotherapy and radiation therapy improves survival compared with surgery alone7,8 or surgery plus radiation therapy.9 In 1990, a Consensus Conference of the National Institutes of Health strongly recommended these adjuvant therapies for patients without medical or psychosocial contraindications.10 Despite these benefits, prior studies have indicated that many potentially eligible patients with colorectal cancer do not receive adjuvant chemotherapy and radiation therapy.11 Among hospital tumor registries in the National Cancer Database, only 46% of patients with stage III colon cancer were reported to receive chemotherapy in 1993.12 In a similar study of rectal cancer during 1994 and 1995, 44% of patients with stage II disease and 59% of those with stage III disease received chemotherapy, and 57% and 62%, respectively, received radiation therapy.13 However, hospital registries may have incomplete data about adjuvant therapy provided in ambulatory settings,14 and they may not be representative of the general population. Studies based on Medicare claims have reported somewhat higher rates of adjuvant therapy,15,16 but these data are typically available only for elderly patients receiving fee-for-service care. Thus they do not include patients who are younger than 65 years or enrolled in Medicare managed care plans, representing nearly half of all patients with colorectal cancer. Claims data also lack information about why adjuvant therapies are not provided to patients with colorectal cancer, and only a few small studies have directly addressed this topic.17–19 To monitor and improve the quality of cancer care in the United States, the National Cancer Policy Board of the Institute of Medicine has recommended substantially enhanced cancer data systems.20 Population-based cancer registries in all 50 states represent a valuable and largely untapped resource for achieving this goal.21 We augmented registry data by surveying physicians about adjuvant therapy for nearly 2,000 eligible patients with colorectal cancer in northern California. Our objectives were to estimate underreporting of adjuvant therapies in routinely collected registry data, assess rates of adjuvant therapies and factors associated with use, and ascertain reasons why eligible patients were not treated.
Study Population The California Cancer Registry is the largest geographically contiguous, population-based cancer registry in the world,22 composed of 10 regional registries that collect incidence, treatment, and survival data on all California residents diagnosed with cancer (except nonmelanoma skin cancers). This study was conducted with three regional registries representing the San Francisco/Oakland, San Jose/Monterey, and Sacramento areas, including 22 counties with approximately 9.3 million people in 1997. These registries have received the highest level of certification from the North American Association of Central Cancer Registries for the completeness, accuracy, and timeliness of their data,23 making them a model for studying the quality of cancer care in community practice. From registry records, we identified all patients 18 years of age and older diagnosed during 1996 and 1997 with stage III adenocarcinoma of the colon or stage II or III adenocarcinoma of the rectum, using staging criteria of the American Joint Committee on Cancer.24 We included patients who had undergone surgical resection and survived at least 30 days. These patients were eligible for adjuvant chemotherapy based on national guidelines, and those with rectal cancer were also eligible for radiation therapy.10 From registry records, we identified a treating physician for 99% of eligible patients. Institutional review boards of the California Department of Health Services, Public Health Institute, Northern California Cancer Center, and Harvard Medical School approved the study protocol in accordance with assurances filed with and approved by the Department of Health and Human Services.
Data Collection To supplement registry data, we designed a brief written survey asking physicians whether their patient received adjuvant chemotherapy or radiation therapy and the specific drugs administered. If a patient did not receive one of these treatments, the physician was asked why it was not given. The survey was mailed from the regional registry to the physician currently following each patient or to the initial attending physician if a current physician was not recorded. Physicians could return the completed survey or have registry staff review their office records. They were also asked to identify other physicians who might know whether patients received chemotherapy or radiation therapy. For patients initially treated in Kaiser Permanente hospitals (23%), registry staff directly reviewed office records under a prior agreement with this health plan. Registry staff sent a second mailing and made numerous telephone calls to nonresponding physicians to enlist their participation. The regional registries provided patients’ cancer stage, age, sex, race/ethnicity, marital status, and Census block group. From the 1990 United States Census, we obtained median household income by race/ethnicity in patients’ block groups, rounded to the nearest $5,000 to maintain confidentiality.25 The 7% of patients without a Census block group (eg, those listing a post office box) were matched to colorectal cancer patients of the same race/ethnicity in their Zip code to obtain multiple imputations of median household income.26,27 Rural areas were designated by the California Health Manpower Policy Commission. Hospitals providing initial treatment were characterized by the annual number of colorectal cancer patients of all stages treated in 1994 through 1997, presence of a tumor registry accredited by the American College of Surgeons Commission on Cancer in 1996,28 and teaching status and availability of radiation therapy as recorded by the Office of Statewide Health Planning and Development. To account for comorbid illnesses, we linked registry data to hospital discharge abstracts maintained by the Office of Statewide Health Planning and Development, using a probabilistic matching algorithm based on patients’ Social Security number, date of birth, sex, and Zip code.29 To maximize ascertainment of relevant comorbid conditions,30 we identified all hospital discharges that occurred within 18 months before or 6 months after patients’ date of diagnosis. We linked at least one abstract for 93% of patients, of which 98% matched exactly by Social Security number. From the principal diagnosis and up to nine secondary diagnoses (not including cancer-related diagnoses) on discharge abstracts, we classified the degree of comorbidity using the Deyo adaptation of the Charlson scale for use with hospital discharge abstracts.31,32 For patients without any linked discharge abstracts (7%), comorbidity was imputed from other available characteristics with standard methods.33,34
Statistical Analysis Adjusted predictors of adjuvant therapy based on combined data from the registries and physicians were assessed with logistic regression models and generalized estimating equations to account for clustering by hospital. In secondary analyses, we tested whether two-way interactions of age with other key variables, including race/ethnicity, sex, and level of comorbidity, predicted use of adjuvant therapy. We also analyzed adjusted predictors of patients’ refusal of chemotherapy among patients who either received or refused this treatment. We report adjusted odds ratios (ORs) and 95% confidence intervals (CIs) from SAS software (version 6.12; SAS Institute, Cary, NC) for adjusted analyses. Using MLwiN software (Center for Multilevel Modeling, London, UK),35 we estimated a hierarchical logistic regression model for chemotherapy accounting for patient and hospital characteristics and random effects of hospitals in which patients were initially treated. The cohort eligible for radiation therapy was too small to support useful estimates from a hierarchical model. We report adjusted rates of chemotherapy at hospitals one SD (on the logit scale) above or below the treatment rate of an average hospital.
Study Population Among 1,956 patients with stage III colon cancer or stage II or III rectal cancer, we obtained treatment information for 1,449 patients (74.1%) from physicians’ surveys (37.7%), office records (25.6%), or both sources (10.8%). Treatment information was obtained less often from physicians’ surveys or office records for patients 75 years of age and older (70% v 76%; P = .02), unmarried patients (71% v 76%; P = .02), nonrural patients (73% v 80%; P = .02), those in low-volume hospitals (61% v 76%; P = .001) or hospitals with radiation facilities (71% v 76%; P = .002), and those in San Francisco/Oakland than in San Jose/Monterey or Sacramento (65%, 74%, 87%; P = .001). The likelihood of receiving information from physicians did not differ statistically by patients’ sex, race/ethnicity, income, cancer stage or site, comorbidity, or hospitals’ registry accreditation, teaching status, or availability of radiation therapy.
Characteristics of patients eligible for chemotherapy and radiation therapy are listed in Table 1
Completeness of Registry Data On the basis of registry data alone, rates of chemotherapy and radiation therapy were 59% and 58%, respectively, among eligible patients. These rates increased to 67% for chemotherapy and 64% for radiation therapy with additional data from physicians’ surveys or office records. Thus, the sensitivity of routinely collected registry data was 87% for chemotherapy and 93% for radiation therapy. If all physicians had responded, we project treatment rates would have increased only slightly to 69% for chemotherapy and 66% for radiation therapy. Only 2% of patients had registry data indicating they had received chemotherapy or radiation therapy but were reported by their physicians not to have received each therapy.
Adjuvant Chemotherapy
In adjusted multivariable analyses accounting for clustering of patients by hospital, older patients were significantly less likely to receive chemotherapy than were younger patients (Table 2  ). Patients with stage II rectal cancer were less likely, and those with stage III rectal cancer were more likely, than patients with stage III colon cancer to receive chemotherapy. Unmarried patients and those with greater comorbidity were significantly less likely than other patients to receive chemotherapy. Relative to the San Francisco/Oakland area, patients in Sacramento were more likely to receive chemotherapy. Sex, race/ethnicity, income, rural residence, and hospital tumor registry accreditation, teaching status, and availability of radiation therapy were not statistically significant adjusted predictors of adjuvant chemotherapy. There were no significant interactions of age with race/ethnicity, sex, or level of comorbidity. In hierarchical models including random effects of individual hospitals, use of chemotherapy varied substantially. Relative to the 67% of patients receiving chemotherapy in the full cohort, the adjusted probability of receiving chemotherapy was 79% in hospitals moderately (one SD) above average and 51% in hospitals moderately below average.
Adjuvant Radiation Therapy
In adjusted analyses, older patients and black patients were significantly less likely to receive radiation therapy than younger patients and white patients, respectively (Table 3 ). Patients with stage II rectal cancer were less likely than those with stage III rectal cancer to receive radiation therapy, as were patients initially treated in low-volume hospitals relative to those in high-volume hospitals. Relative to patients in the San Francisco/Oakland area, patients in San Jose/Monterey were less likely to receive radiation therapy. Sex, income, rural residence, and hospital registry accreditation, teaching status, and availability of radiation therapy were not significant predictors of this treatment. No significant interactions of age with race/ethnicity, sex, or level of comorbidity were evident. In an adjusted analysis limited to patients with rectal cancer, the combination of radiation therapy and chemotherapy was delivered significantly more often to patients younger than 55 years of age (OR, 2.7; 95% CI, 1.3 to 5.6) and less often to patients 75 to 84 years of age (OR, 0.3; 95% CI, 0.2 to 0.5) and 85 years of age and older (OR, 0.1; 95% CI, 0.0 to 0.2), relative to patients 65 to 74 years of age. Asian patients were more likely than white patients to receive combined adjuvant therapy (OR, 2.0; 95% CI, 1.0 to 3.7). Combined therapy was administered less often to patients with stage II disease than to those with stage III disease (OR, 0.5; 95% CI, 0.3 to 0.7) or in low-volume hospitals relative to high-volume hospitals (OR, 0.4; 95% CI, 0.2 to 0.9).
Reasons for Not Administering Adjuvant Therapies
The distribution of these reasons differed substantially by patient age (Table 4 ). Among patients 85 years of age and older who did not receive adjuvant chemotherapy, physicians commonly reported comorbid illnesses and advanced age as reasons it was not administered. Physicians were much more likely to report chemotherapy was not indicated for stage II rectal cancer (42%) than for stage III cancers of the colon or rectum (16% and 17%, respectively; P = .001), but they viewed radiation therapy as not indicated for similar proportions of untreated patients with stage II or III rectal cancer (47% v 43%; P = .41).
Among patients who were apparently offered chemotherapy (ie, either received or refused it), the unadjusted refusal rate was substantially lower for younger patients than for older patients (5% for age < 65 years, 10% for age 65 to 74 years, 20% for age 75 to 84 years, and 46% for age
In this population-based study of patients diagnosed with colorectal cancer during 1996 and 1997 in northern California, two thirds of patients potentially eligible for adjuvant chemotherapy or radiation therapy received these treatments. Although some patients will refuse these treatments or have clear clinical contraindications, we would expect treatment rates of 80% or greater are attainable in community practice, as we found for chemotherapy among patients initially treated at above-average hospitals in our study. Patient age was the strongest predictor of adjuvant therapy, consistent with prior studies.15–18,36–39 Among patients 75 years of age and older, representing one third of our cohort, comorbidity and advanced age were much more commonly cited reasons for not administering adjuvant therapies than was patient refusal. However, steep age gradients were evident even among patients with little or no evidence of comorbidity in hospital discharge abstracts. Physicians may have reasonable concerns about poor outcomes in older patients with colorectal cancer and other chronic illnesses,40 but randomized trials and observational studies demonstrate that older patients with colon cancer and good functional status experience survival benefits of chemotherapy similar to those of younger patients.41–43 Our findings underscore the need for randomized clinical trials and rigorous observational studies to assess the benefits and risks of adjuvant therapy for colorectal cancer among older patients, including those with comorbid conditions.44,45 The racial and ethnic diversity of northern California enabled us to assess treatment of colorectal cancer in multiple racial and ethnic groups, thereby building on a limited number of prior studies.11,39 In adjusted analyses, Hispanic and Asian patients did not differ statistically from white patients in their rates of chemotherapy or radiation therapy. Black patients were significantly less likely than white patients to receive radiation therapy, but not chemotherapy. Future studies should assess why black patients are less likely to receive radiation therapy and develop interventions to eliminate such differences in care.46 Married patients had higher adjusted rates of chemotherapy than unmarried patients in our cohort, possibly reflecting spouses’ encouragement of patients to seek additional therapy and their ability to provide transportation to medical appointments. Other studies have also found associations between marital status and more comprehensive cancer care.39,47,48 Referring unmarried patients to medical oncologists will help ensure that chemotherapy is administered when indicated.36 The wide variation in adjusted rates of chemotherapy across individual hospitals, lower rates of radiation therapy in low-volume hospitals, and regional differences for both therapies underscore the influence of institutional factors and local practice patterns in determining the use of adjuvant therapies.49–51 Many physicians did not believe that chemotherapy was indicated for stage II rectal cancer or that radiation therapy was indicated for stage II or III rectal cancer. In a prior study in Sacramento, CA, patients with proximal rectal tumors were much less likely to receive combined adjuvant chemotherapy and radiation therapy than those with more distal tumors, indicating that physicians may treat many proximal rectal tumors according to published guidelines for colon cancer rather than rectal cancer.38 Understanding how physicians incorporate patients’ tumor characteristics and comorbidity in treatment recommendations may help to refine estimates of potential underuse of adjuvant therapies relative to current guidelines. Identifying hospitals with low rates of adjuvant therapies that are unexplained by clinical factors may stimulate efforts to promote more appropriate cancer treatment. The completeness of California Cancer Registry data on chemotherapy and radiation therapy was substantially greater than previously described for individual hospital registries in New York,14 indicating that population-based registries can obtain data more readily than hospital registries from sites of ambulatory care. Among 211 patients with stage III colon cancer in Illinois, Kentucky, and Louisiana during 1997, chemotherapy rates increased from 41% to 53% when state cancer registry data were supplemented with additional data from oncologists.52 For patients 65 years of age and older, use of adjuvant chemotherapy and radiation therapy in our study were similar to rates derived from Medicare claims in northern California during 1991 through 1996,15,16 indicating that either physicians or Medicare claims can enhance the accuracy of registry data.53–55 For the 2% of patients in our study whose registry data indicated that they had received adjuvant therapy but their physician did not concur, the responding physician may have been unaware of treatment delivered by another physician that was known to the registry. Strengths of our study included the large representative cohort and relatively high response (74%) from physicians to provide additional treatment data. Our study was conducted with well-established regional cancer registries, so our analyses should be replicated in other areas. We did not analyze the duration or intensity of adjuvant therapy, directly evaluate the clinical appropriateness of decisions about adjuvant therapy, or ask patients whether they had been offered adjuvant therapies or had chosen not to receive them. Our findings indicate that adjuvant chemotherapy and radiation therapy may be underused for eligible patients with colorectal cancer, well after an evidence-based national consensus statement strongly endorsed these treatments. Because lower rates of adjuvant therapy were concentrated in elderly patients, including those with and without substantial comorbidity, further research is warranted to determine the benefits and risks of adjuvant therapy for these patients. In contrast, differences in treatment by race, marital status, or hospital have no clear clinical rationale and represent opportunities to reduce disparities in quality of care. By supplementing population-based cancer registries with additional data on ambulatory treatments, these registries may be used more broadly to monitor and improve the quality of cancer care in the United States.
We thank Craig Grilley and Scott Riddle for assistance with database management, Martha Felter, CTR, for assistance with collecting data from physicians, and Calvin W.F. Chiu and Recai Yucel, PhD, for imputing missing income and comorbidity data.
This study was supported by a grant from the Agency for Healthcare Research and Quality and the National Cancer Institute (grant R01 HS09869). The views expressed in this article are those of the authors and do not necessarily reflect official positions of the California Department of Health Services or the Public Health Institute.
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Copyright © 2003 by the American Society of Clinical Oncology, Online ISSN: 1527-7755. Print ISSN: 0732-183X
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ABSTRACT
INTRODUCTION
85 years), and radiation therapy varied similarly. Adjusting for demographic, clinical, and hospital characteristics, chemotherapy was used less often among older and unmarried patients, and radiation therapy was used less often among older patients, black patients, and those initially treated in low-volume hospitals. Adjusted rates of chemotherapy varied significantly (P < .01) among individual hospitals: 79% and 51%, respectively, at one SD above and below average (67%). Physicians’ reasons for not providing adjuvant therapy included patient refusal (30% for chemotherapy, 22% for radiation therapy), comorbid illness (22% and 14%, respectively), or lack of clinical indication (22% and 45%, respectively). 
