Racial Differences in the Receipt of Bowel Surveillance Following Potentially Curative Colorectal Cancer Surgery
To investigate racial differences in posttreatment bowel surveillance after colorectal cancer surgery in a large population of Medicare patients. We used a large population-based dataset: Surveillance, Epidemiology, and End Results (SEER) linked to Medicare data. This is a retrospective cohort study. We analyzed data from 44,768 non-Hispanic white, 2,921 black, and 4,416 patients from other racial/ethnic groups, aged 65 and older at diagnosis, who had a diagnosis of local or regional colorectal cancer between 1986 and 1996, and were followed through December 31, 1998. Cox Proportional Hazards models were used to investigate the relation of race and receipt of posttreatment bowel surveillance. Sociodemographic, hospital, and clinical characteristics were collected at the time of diagnosis for all members of the cohort. Surgery and bowel surveillance with colonoscopy, sigmoidoscopy, and barium enema were obtained from Medicare claims using ICD-9-CM and CPT-4 codes. The chance of surveillance within 18 months of surgery was 57 percent, 48 percent, and 45 percent for non-Hispanic whites, blacks, and others, respectively. After adjusting for sociodemographic, hospital, and clinical characteristics, blacks were 25 percent less likely than whites to receive surveillance if diagnosed between 1991 and 1996 (RR = 0.75, 95 percent CI = 0.70-0.81). Elderly blacks were less likely than non-Hispanic whites to receive posttreatment bowel surveillance and this result was not explained by measured racial differences in sociodemographic, hospital, and clinical characteristics. More research is needed to explore the influences of patient- and provider-level factors on racial differences in posttreatment bowel surveillance.
Racial Differences in the Receipt of
Bowel Surveillance Following Potentially
Curative Colorectal Cancer Surgery
Gary L. Ellison, Joan L. Warren, Kevin B. Knopf, and Martin L.
Objective. To investigate racial differences in posttreatment bowel surveillance after
colorectal cancer surgery in a large population of Medicare patients.
Data Sources. We used a large population-based dataset: Surveillance, Epidemiology,
and End Results (SEER) linked to Medicare data.
Study Design. This is a retrospective cohort study. We analyzed data from 44,768
non-Hispanic white, 2,921 black, and 4,416 patients from other racial/ethnic groups,
aged 65 and older at diagnosis, who had a diagnosis of local or regional colorectal cancer
between 1986 and 1996, and were followed through December 31, 1998. Cox
Proportional Hazards models were used to investigate the relation of race and receipt of
posttreatment bowel surveillance.
Data Collection. Sociodemographic, hospital, and clinical characteristics were
collected at the time of diagnosis for all members of the cohort. Surgery and bowel
surveillance with colonoscopy, sigmoidoscopy, and barium enema were obtained from
Medicare claims using ICD-9-CM and CPT-4 codes.
Principal Findings. The chance of surveillance within 18 months of surgery was 57
percent, 48 percent, and 45 percent for non-Hispanic whites, blacks, and others,
respectively. After adjusting for sociodemographic, hospital, and clinical characteristics,
blacks were 25 percent less likely than whites to receive surveillance if diagnosed
between 1991 and 1996 (RR 5 0.75, 95 percent CI 5 0.70–0.81).
Conclusions. Elderly blacks were less likely than non-Hispanic whites to receive
posttreatment bowel surveillance and this result was not explained by measured racial
differences in sociodemographic, hospital, and clinical characteristics. More research is
needed to explore the inﬂuences of patient- and provider-level factors on racial
differences in posttreatment bowel surveillance.
Key Words. Colorectal neoplasms, SEER-Medicare, colonoscopy, blacks, surveil-
Colorectal cancer is the second leading cause of cancer mortality in the United
States and is estimated to account for 56,600 deaths in 2002 ( Jemal et al. 2002).
Important racial and ethnic differences exist in colorectal cancer incidence
and mortality. While U.S. blacks have a 12 percent higher incidence rate than
U.S. whites, the black mortality rate is 36 percent higher (Ries et al. 2002).
Incidence and mortality rates for members of other racial/ethnic groups are
similar to or lower than those of U.S. whites. Moreover, survival following
potentially curative treatment is often worse for blacks than for whites
regardless of socioeconomic status, tumor, or treatment characteristics
(Mayberry et al. 1995; Cooper et al. 1996).
Most newly diagnosed colorectal cancer cases will have surgery with
curative intent (Decosse, Tsioulias, and Jacobson 1994; Rosen et al. 1998).
Patients receiving surgery after an initial diagnosis of colorectal cancer are at
increased risk of recurrence and metachronous tumors. The risk of recurrence
increases substantially with increasing stage of disease. Consequently,
recurrence occurs in 35 to 40 percent of patients presented with stage II or
III disease; most recurrences occur within three years after primary surgery
(Desch et al. 1999). Metachronous or second primary tumors occur at a rate of
0.35 percent per year (Virgo et al. 1995), and the risk is higher among younger
(o65 years) than among older age groups (Shureiqi et al. 2001).
Because patients receiving potentially curative colorectal cancer surgery
are at risk of recurrence and increased risk of developing second primary
tumors, posttreatment bowel surveillance is recommended to detect these
tumors at earlier and more curable stages. Based on the best available
evidence regarding posttreatment surveillance, professional societies have
established guidelines to aid clinicians in treating these high-risk patients.
Clinical guidelines vary with regard to intensity and frequency of posttreat-
ment surveillance, but most suggest initial posttreatment surveillance with
colonoscopy or barium enema within one year of surgery with curative intent
and at three to ﬁve years following the initial surveillance (Desch et al. 1999;
Fleischer et al. 1989; Virgo et al. 1995).
Clinical guidelines may be useful in minimizing inappropriate variation
in practice (Desch et al. 1999). However, despite recommendations of
professional societies, studies have documented wide variations in actual
practice with regard to physician reporting (Virgo et al. 1995; Vernava et al.
1994) and receipt (Cooper et al. 1999, 2000; Elston Lafata et al. 2001; Knopf et
al. 2001) of surveillance procedures. Consequently, clinical guidelines do not
Address correspondence to Gary L. Ellison, Ph.D., M.P.H., Macro International, QRC Division,
7315 Wisconsin Avenue, Suite 400W, Bethesda, MD, 20814-3202. Joan L. Warren, Ph.D., and
Martin L. Brown, Ph.D., are with the Health Services and Economics Branch, Applied Research
Program, Division of Cancer Control and Population Sciences, National Cancer Institute,
Bethesda, MD. Kevin B. Knopf, M.D., M.P.H., is with the Annapolis Oncology/Hematology
Center, Annapolis, MD.
1886 HSR: Health Services Research 38:6, Part II (December 2003)
always account for individual variation among patients and adherence is often
a function of a physician’s determination of need based on clinical and
nonclinical circumstances, as well as patient preferences.
While many studies document racial disparities in cancer treatment,
there are relatively few studies that look at care following initial therapy. The
studies that investigated posttreatment bowel surveillance are limited in the
data and analytical approaches used. Cooper et al. (1999, 2000) found
geographic, but not racial differences among Medicare beneﬁciaries
diagnosed during a single year. This study did not account for censoring in
the analysis. In a health maintenance organization (HMO) population
diagnosed over a six-year period, racial and socioeconomic differences in
posttreatment surveillance were observed, but these ﬁndings were from a
single HMO with a small sample size and the results did not reach statistical
signiﬁcance with regard to racial differences (Elston Lafata et al. 2001). In
addition, the previous studies had insufﬁcient data to monitor changes in racial
disparities over time. As in the case of breast cancer screening, it might be
thought that disparities in posttreatment surveillance are decreasing over time.
This study is unique in being able to investigate that question in a particularly
reliable manner because it uses a large longitudinal database.
The objective of the current analysis is to investigate racial differences
among Medicare beneﬁciaries in the receipt of bowel surveillance procedures
following colorectal cancer surgery with curative intent, while accounting for
racial differences in sociodemographic, hospital, and clinical characteristics.
This analysis takes advantage of the SEER-Medicare linked database that is
large, national in scope, and population-based.
We used data from the National Cancer Institute’s (NCI) Surveillance,
Epidemiology, and End Results (SEER) program for colorectal cancer cases
diagnosed from 1986 through 1996 linked to Medicare claims data through
1998) (http://healthservices.cancer.gov/seermedicare/) (Warren et al. 2002).
The SEER is a population-based system of cancer registries that collects
incident and survival data on all cancers in six metropolitan areas (San
Francisco/Oakland, Detroit, Atlanta, Seattle, Los Angeles, San Jose) and ﬁve
states (Connecticut, Utah, New Mexico, Iowa, Hawaii), and covers
approximately 14 percent of the U.S. population. Data from SEER include
Racial Differences in the Receipt of Bowel Surveillance 1887
site of the tumor, stage, and histology, as well as the initial course of treatment.
Information on posttreatment procedures is not maintained in SEER.
The Medicare program, administered by the Center for Medicare and
Medicaid Services (CMS), formerly known as the Health Care Financing
Administration, provides health insurance coverage to approximately 97
percent of individuals aged 65 and older in the United States. Medicare claims
are contained in the Medicare Provider Analysis and Review (MedPAR) ﬁles
and contain up to 10 diagnoses and 10 procedures for all billed claims coded
using both ICD-9-CM diagnoses and CPT-4 procedure codes. These codes
facilitate identiﬁcation of patients who receive surgery for colorectal cancer
and posttreatment surveillance activities following potentially curative
Details regarding the assembly of the cohort used in this analysis have been
described elsewhere (Knopf et al. 2001). Brieﬂy, the cohort consisted of
patients who had a diagnosis of adenocarcinoma of the colon or rectum,
diagnosed at the local (tumor-node-mestastasis [TNM] Stages I or II) or
regional (TNM Stage III) stages between January 1, 1986, and October 31,
1996, and who underwent surgery with curative intent. We excluded patients
diagnosed with colorectal cancer before age 65, diagnosed by death certiﬁcate
or autopsy, or who did not have a month or year of diagnosis. Patients with a
prior or concurrent diagnosis of any noncutaneous malignancy were also
excluded, as well as were patients diagnosed with colorectal cancer in situ,
Crohn’s disease, and ulcerative colitis. Finally, Medicare beneﬁciaries
enrolled in an HMO before their cancer diagnosis were excluded because
Medicare does not cover HMO claims. The analytic cohort consisted of
52,105 patients diagnosed with local or regional adenocarcinoma of the colon
Once the cohort was deﬁned, we searched Medicare claims records for
patients who had colorectal cancer surgery within two months of the SEER
month and year of diagnosis to determine an index date of initial surgery. We
sequentially searched the hospital, outpatient, and physician claims ﬁles for
the presence of a cancer-directed surgery or procedure and assigned a date of
Each patient was followed from the date of initial colorectal surgery,
until censored, or until December 31, 1998, the last date for which Medicare
claims data were available. Patients were censored if they lost Medicare A/B
1888 HSR: Health Services Research 38:6, Part II (December 2003)
entitlement after their index date or enrolled in an HMO after their colorectal
cancer diagnosis. In addition, patients were censored if they were enrolled in a
hospice after the index date. Patients who died during the follow-up period
were censored six months prior to their date of death. Also censored were
patients who developed a noncutaneous malignancy other than their index
diagnosis of colorectal cancer, a second colorectal cancer primary, as reported
by SEER, and patients who developed recurrent colorectal cancer.
We searched the Medicare claims for all bowel surveillance procedures from
the index date until the date of censoring or December 31, 1998. We excluded
any surveillance procedures occurring during the ﬁrst two months after
treatment to ensure that perioperative procedures were not counted. Bowel
surveillance procedures studied were colonoscopy, sigmoidoscopy, endo-
scopy, and barium enema. ICD-9-CM and CPT-4 codes for these procedures
are detailed elsewhere (Knopf et al. 2001).
Sociodemographic, hospital, and clinical characteristics were collected at
baseline for all members of the cohort. Sociodemographic variables included
SEER race, gender, age at diagnosis, SEER registry, as a measure of
geographic region, and education measured at the level of the census tract.
Clinical variables included the Charlson comorbidity index, which is a
weighted index that takes into account the number and seriousness of
comorbid conditions (Charlson et al. 1987; Deyo, Cherkin, and Ciol 1992).
We examined inpatient, outpatient, and hospital claims for the presence of
comorbid conditions 12 months before diagnosis. We also included stage at
diagnosis obtained from SEER as a covariate. We used the American Hospital
Association data to determine characteristics about the hospital treating the
patients. These variables include hospital ownership (government, nonproﬁt,
and for-proﬁt), hospital bed size, and afﬁliations with the American College of
Surgeons and Council of Teaching Hospitals, which were used to characterize
the type of hospital patients received services.
The racial distributions of patient characteristics were compared using chi-
square tests. Time to ﬁrst posttreatment surveillance for each racial category
was assessed using Kaplan-Meier (K-M) curves, and the log-rank test was used
Racial Differences in the Receipt of Bowel Surveillance 1889
to investigate statistical differences in posttreatment surveillance between
racial groups. Graphs were plotted as the cumulative proportion of individuals
having a posttreatment surveillance event with time since surgery with
curative intent. Unconditional logistic regression was used to estimate odds
ratios for the effect of race on type of posttreatment bowel surveillance
received and to adjust for multiple covariates. We used Cox proportional
hazards models to estimate hazard ratios for race and time to ﬁrst
posttreatment surveillance while adjusting for sociodemographic, hospital,
and clinical covariates. Standard errors of the Cox regression coefﬁcients were
used to calculate 95 percent conﬁdence intervals. The ﬁnal model was used to
predict the probability of posttreatment surveillance at 18, 36, and 60 months
after surgery with curative intent for each racial category based on the mean
sociodemographic, hospital, and clinical covariate distribution of non-
Hispanic whites (Allison 1995). We repeated the analysis for race and time
from ﬁrst to second posttreatment bowel surveillance, as well as for subsequent
bowel surveillance during follow-up. All analyses were performed using the
SAS version 8.2 statistical software package (SAS Institute 2001).
We analyzed data from non-Hispanic white (n 5 44,768), black (n 5 2,921),
and members of other racial groups (n 5 4,416) who had a colorectal cancer
diagnosis between January 1, 1986, and October 31, 1996. The racial
distributions of patient characteristics are shown in Table 1. Statistically
signiﬁcant racial differences existed for most baseline covariates; some of the
differences are small, yet statistically signiﬁcant due to the very large sample
size. Non-Hispanic whites and blacks had a larger proportion of females. Non-
Hispanic whites tended to be older than other groups at diagnosis. A higher
proportion of other racial groups were diagnosed in the later years of the study
than were blacks and non-Hispanic whites. Blacks tended to have higher
comorbidity scores, although in general, more minorities than non-Hispanic
whites were missing these data. Blacks were overrepresented in communities
where a signiﬁcant proportion of residents lacked a high school diploma.
Members of other racial groups were more likely than non-Hispanic whites
and blacks to attend for-proﬁt institutions, while blacks were more likely to
receive treatment at larger hospitals that were afﬁliated with the American
College of Surgeons and Council of Teaching Hospitals.
1890 HSR: Health Services Research 38:6, Part II (December 2003)
Table 1: Colorectal Cancer Patient Characteristics, SEER-Medicare,
Non-Hispanic White Black Other
(N 5 44,768) (N 5 2,921) (N 5 4,416)
Characteristics % % %
Male 47.1 43.3 54.4
Female 52.9 56.7 45.6
Age at Diagnosis
65–69 22.0 28.2 29.3
70–74 25.0 28.3 28.0
75–79 23.6 22.4 20.5
80–84 17.3 13.0 14.2
851 12.1 8.1 8.0
Year of Diagnosis
1986 8.4 7.0 5.9
1987 8.4 7.1 5.9
1988 8.7 7.9 6.5
1989 8.9 6.7 7.7
1990 8.9 8.3 7.5
1991 8.8 9.1 8.4
1992 10.5 11.9 11.9
1993 10.3 10.9 11.7
1994 10.1 12.6 13.2
1995 9.3 10.6 12.4
1996 7.7 7.8 8.8
Geographic Region of Residence
Atlanta 4.4 14.9 0.7
Connecticut 17.4 7.8 3.1
Detroit 14.8 40.0 1.3
Hawaii 1.1 0.2 32.0
Iowa 18.9 1.9 0.5
Los Angeles 7.5 13.7 19.1
New Mexico 3.3 0.9 10.0
San Francisco/Oakland/San Jose 15.7 17.5 27.6
Seattle/Puget Sound 12.9 2.9 4.1
Utah 4.1 0.2 1.5
Percent of Census-tract without High School
Lowest quartile 26.5 5.6 17.2
2nd quartile 20.8 6.8 15.4
3rd quartile 22.7 17.2 18.2
Highest quartile 17.3 55.4 22.2
Missing 12.7 15.0 27.0
Racial Differences in the Receipt of Bowel Surveillance 1891
A graphical display of posttreatment bowel surveillance after colorectal
cancer surgery with curative intent is shown in Figure 1. There were
statistically signiﬁcant racial differences in time to ﬁrst posttreatment bowel
surveillance (log-rank test, po0.001). Fifty-seven percent of whites, 48 percent
of blacks, and 45 percent of others received posttreatment surveillance within
Table 1: Continued
Non-Hispanic White Black Other
(N 5 44,768) (N 5 2,921) (N 5 4,416)
Characteristics % % %
Government 11.8 7.9 12.9
Nonproﬁt 79.5 82.7 70.1
For Proﬁt 5.6 4.6 9.8
Missing 3.2 4.7 7.2
6–199 32.4 12.6 44.2
200–399 38.0 32.6 38.3
4001 26.4 50.1 10.4
Missing 3.2 4.7 7.2
American College of Surgeons
Yes 57.4 59.9 60.7
No 39.4 35.4 32.1
Missing 3.2 4.7 7.2
Council of Teaching Hospitals
Yes 20.3 45.1 9.6
No 76.6 50.2 83.2
Missing 3.2 4.7 7.2
Charlson Comorbidity Score
0 58.4 53.7 55.9
1 21.3 20.3 18.1
Z2 7.7 9.5 6.1
12.7 16.5 19.9
Localized 53.7 51.7 53.1
Regional 46.3 48.3 46.9
Percent of census-tract without high school diploma categories: Lowest quartile, r15.75; 2nd
quartile, 15.76–24.76; 3rd quartile, 24.77–35.4; highest quartile, Z35.5.
Unable to calculate Charlson Comorbidity Score for missing records.
Not statistically signiﬁcant.
1892 HSR: Health Services Research 38:6, Part II (December 2003)
18 months of potentially curative surgery. These racial differences remained at
the end of three years (67, 61, and 56 percent) and at the end of ﬁve years (74,
70, and 63 percent) after surgery for whites, blacks, and others, respectively.
The Cox proportional hazards models, adjusted for sociodemographic,
hospital, and clinical characteristics, for time to ﬁrst bowel surveillance are
shown in Table 2. The rate of posttreatment bowel surveillance was greater for
individuals in all racial groups diagnosed between 1991 and 1996 than if
diagnosed between 1986 and 1990, and racial differences in posttreatment
bowel surveillance existed within those years of diagnosis. Accordingly, the
relationship between race and time to ﬁrst posttreatment bowel surveillance
was modiﬁed by year of diagnosis (p 5 0.008). If diagnosed between 1986 and
1990, blacks were 13 percent and patients in other racial groups were 8
percent less likely than non-Hispanic whites to receive posttreatment bowel
surveillance, independent of sociodemographic, hospital, and clinical
characteristics (RR 5 0.87, 95 percent CI 5 0.80–0.94; RR 5 0.91, 95 percent
CI 5 0.84–1.00 for blacks and others, respectively). If diagnosed between
1991 and 1996, blacks compared with non-Hispanic whites were 25 percent
less likely to have received posttreatment surveillance (RR 5 0.75, 95 percent
CI 5 0.70–0.81). No statistically signiﬁcant differences in posttreatment bowel
0 20 40 60 80 100 120 140 16
Months Since Index Date
Chance of Surveillance
Figure 1: Time to Receipt of a First Bowel Surveillance Procedure Following
Potentially Curative Surgery, SEER-Medicare: 1986–1998
Racial Differences in the Receipt of Bowel Surveillance 1893
Table 2: Adjusted Cox Proportional Hazards Models for Time to First Bowel Surveillance Following Potentially
Curative Surgery, SEER-Medicare: 1986–1998
Bivariate Model 1 Model 2 Model 3
RR 95% CI RR 95% CI RR 95% CI RR 95% CI
Non-Hispanic White 1.0 Reference 1.0 Reference 1.0 Reference 1.00 Reference
Black 0.89 0.83–0.96 0.83 0.77–0.90 0.83 0.77–0.90 0.87 0.80–0.95
Other 0.64 0.60–0.69 0.89 0.82–0.96 0.90 0.83–0.98 0.91 0.84–1.00
Non-Hispanic White 1.0 Reference 1.0 Reference 1.0 Reference 1.0 Reference
Black 0.78 0.74–0.83 0.75 0.70–0.80 0.75 0.70–0.80 0.75 0.70–0.81
Other 0.75 0.71–0.79 1.00 0.93–1.07 1.02 0.95–1.10 0.99 0.92–1.07
Model 1 adjusts for sociodemographic characteristics; Model 2 adjusts for sociodemographic and hospital characteristics; Model 3 adjusts for
sociodemographic, hospital, and clinical characteristics.
1894 HSR: Health Services Research 38:6, Part II (December 2003)
Table 3: Adjusted
Probability of Bowel Surveillance within 18, 36, and 60 Months, SEER-Medicare, 1986–1998
Diagnosed 01/01/86 to 12/31/90 Diagnosed 01/01/91 to 10/31/96
Within 18 Months Within 36 Months Within 60 Months Within 18 Months Within 36 Months Within 60 Months
Race 95% CI 95% CI 95% CI 95% CI 95% CI 95% CI
Non-Hispanic White 51.7 66.4 75.8 64.8 75.1 79.9
50.9–52.4 65.6–67.2 75.0–76.6 63.4–66.2 73.7–76.4 78.6–81.2
Black 47.8 62.3 71.9 54.4 64.8 70.2
44.9–50.6 59.1–65.3 68.7–74.8 51.6–57.1 61.9–67.6 67.2–72.9
45.7–52.4 59.9–67.2 69.6–76.5 59.9–66.0 70.4–76.3 75.5–81.1
Adjusted for mean sociodemographic, hospital, and clinical characteristics of non-Hispanic whites at diagnosis.
Racial Differences in the Receipt of Bowel Surveillance 1895
surveillance between non-Hispanic whites and patients of other racial groups
were observed when we adjusted for sociodemographic, hospital, and clinical
covariates. Differences in posttreatment bowel surveillance between blacks
and non-Hispanic whites remained regardless of sociodemographic, hospital,
and clinical characteristics.
More than 70 percent of the bowel surveillance procedures received
were colonoscopy; however, this proportion also differed by race. Blacks were
almost 40 percent more likely than non-Hispanic whites to receive
posttreatment bowel surveillance with barium enema when adjusted for
sociodemographic, hospital, and clinical covariates (OR 5 1.39, 95 percent
CI 5 1.18–1.63). We did not observe a statistically signiﬁcant difference in the
type of posttreatment bowel surveillance received between non-Hispanic
whites and others.
We used the Cox proportional hazards model, adjusted for the mean
baseline sociodemographic, hospital, and clinical covariate distribution of
non-Hispanic whites, to predict the probability of receiving posttreatment
bowel surveillance by 18, 36, and 60 months following the index date. The
probability of receiving posttreatment bowel surveillance by month 18, if
diagnosed between 1986 and 1990, was 51, 48, and 49 percent for non-
Hispanic whites, blacks, and others, respectively. By the end of the ﬁfth year
after diagnosis, the probability of receiving posttreatment bowel surveillance
increased to more than 70 percent for all racial groups. If diagnosed between
1991 and 1996, the probability of receiving posttreatment surveillance by 18
months after diagnosis was 64, 54, and 62 percent for non-Hispanic whites,
blacks, and others, respectively. The difference in the probability of receiving
posttreatment bowel surveillance between non-Hispanic whites and blacks
increased substantially over the two periods of diagnosis (Table 3).
We observed statistically signiﬁcant racial differences in the rate of
posttreatment bowel surveillance (log-rank, p 5 0.02) after having received a
ﬁrst procedure (data not shown). Although statistically signiﬁcant, most likely
due to the large sample size, this result may not be clinically meaningful.
When adjusted for sociodemographic, hospital, and clinical characteristics,
blacks were 9 percent less likely than non-Hispanic whites to receive a second
posttreatment bowel surveillance procedure (RR 5 0.91; 95 percent
CI 5 0.85–0.98). No differences in subsequent posttreatment bowel surveil-
lance were observed between non-Hispanic whites and others. This result did
not vary by the time of diagnosis. We did not observe racial differences in
receipt of the third posttreatment bowel surveillance procedure (log-rank,
p 5 0.44).
1896 HSR: Health Services Research 38:6, Part II (December 2003)
In a large cohort of more than 52,000 Medicare beneﬁciaries, we found
statistically signiﬁcant racial differences in posttreatment bowel surveillance
after potentially curative colorectal cancer surgery, with blacks being less
likely than non-Hispanic whites to receive follow-up surveillance. The
observed racial variation in posttreatment bowel surveillance increased
slightly after we adjusted for differences in measured sociodemographic,
hospital, and clinical characteristics. We also observed that the probability of
receiving bowel surveillance increased over time for all racial groups, and the
difference in actual receipt between black and white patients also increased.
Because the initial dissemination of clinical guidelines coincides with the most
recent period of observation, it may be too soon to expect the guidelines to
have a signiﬁcant impact on practice (Knopf et al. 2001), although they may
have some impact on the increasing receipt of the ﬁrst posttreatment bowel
surveillance over time. These data are over three years old, and it is probable
that, as clinical guidelines become more widely disseminated, this increasing
trend as speciﬁed by guidelines will continue. However, it is not clear why, in
light of the increasing trend of posttreatment bowel surveillance receipt, the
racial disparity in use also increased over time.
Other studies have identiﬁed racial differences in the receipt and quality
of care for a variety of conditions (Cooper et al. 1996; Lee et al. 1997;
McMahon et al. 1999; Jencks et al. 2000; Gornick 2000; Mayberry, Mili, and
Oﬁli 2000; Institute of Medicine 2002; Shavers and Brown 2002). Racial
disparities in the use of postdiagnostic surveillance among Medicare
beneﬁciaries with cancer have been observed in other types of cancers
(Schrag et al. 2003; Schapira, McAuliffe, and Nattinger 2000). However, while
these differences have been noted, the reasons for these differences are not
well understood. These differences may be the result of problems with access
to care or reﬂect differences in perception between white and black patients or
providers regarding posttreatment bowel surveillance.
This study was limited to the Medicare fee-for-service population,
therefore, everyone in the cohort had health insurance. However, being
Medicare-eligible does not totally eliminate ﬁnancial access barriers because
Medicare imposes deductibles and copayments on its beneﬁciaries. Expensive
procedures, such as colonoscopy, would result in signiﬁcant copayments for
those persons who do not carry supplemental insurance to cover charges not
reimbursed by Medicare. Whereas 28 percent of whites have Medigap
supplemental coverage, only 7.4 percent of blacks have this coverage (Super
Racial Differences in the Receipt of Bowel Surveillance 1897
2002). We used the educational attainment of the census-tract to adjust for
socioeconomic status in the analysis, but socioeconomic status failed to
explain racial differences in the receipt of bowel surveillance. We were unable
to assess from these data whether individual-level socioeconomic status played
a role in gaining access to bowel surveillance. Financial access, measured by
individual-level patient variables, should be explored as a possible barrier to
the receipt of routine posttreatment bowel surveillance.
In addition to issues related to ﬁnancial access to care, there might be
other issues related to access to care that explain the disparities in surveillance.
For example, colonoscopy must be performed by specialists in facilities that
are adequately equipped to provide conscious sedation. Blacks may be more
likely to reside in places that have fewer physicians or facilities that offer
colonoscopy. However, we observed that once a person underwent the ﬁrst
posttreatment bowel surveillance procedure, racial differences were minimal
and disappeared altogether by the receipt of subsequent procedures. This
ﬁnding suggests that once a person accesses surveillance, he or she is more
likely to continue to receive follow-up.
Our data source is limited in its ability to discern if differential receipt of
posttreatment bowel surveillance reﬂects differences by race in a patient’s
perception related to posttreatment surveillance and if the patient’s perception
is inﬂuenced by the provider’s recommendations. A patient’s experience
during the initial cancer treatment, attitude regarding the need for follow-up,
and trust of the recommendations from the physician may inﬂuence the use of
posttreatment surveillance. There is evidence that physician–patient race
concordance is associated with greater participation in care processes, higher
patient satisfaction, and greater adherence to treatment (Cooper-Patrick et al.
1999; LaVeist and Nuru-Jeter 2002; LaVeist and Carroll 2002), but it is
unclear whether it leads to receipt of standard care.
The provider has signiﬁcant inﬂuence on rates of postdiagnostic
surveillance. Earlier studies have shown that the specialty of the provider
has an impact on recommendations regarding testing (Burns et al. 1997). It is
plausible that black patients were more likely than white patients to seek
follow-up care from general practitioners who may recommend different
practices regarding postdiagnostic surveillance than do specialists. This
difference may explain the fact that blacks received the lower-quality barium
enema (Winawer et al. 2000) more often than non-Hispanic whites, although
we cannot determine the reason for this from these data. Future research
should consider how physician type and physician–patient race concordance
1898 HSR: Health Services Research 38:6, Part II (December 2003)
inﬂuences racial differences in the receipt of posttreatment bowel surveillance
Our study is consistent with other studies that identiﬁed variation in
posttreatment bowel surveillance. Using a SEER-Medicare database of 5,716
patients diagnosed with colorectal cancer in 1991, Cooper et al. (1999, 2000)
found statistically signiﬁcant geographic variations in the use of a variety of
posttreatment surveillance procedures, including colonoscopy and barium
enema. They did not, however, observe racial variations in the receipt of
posttreatment procedures. That study used data from Medicare beneﬁciaries
who were diagnosed during a single year and did not account for the censoring
of observations in determining rates of procedure use; these differences in
sample sizes and analyses methods may have explained the differences
observed in posttreatment bowel surveillance by race. In a managed care
population of 251 individuals in southeast Michigan, diagnosed with
colorectal cancer between 1990 and 1995, aged 40 and older at diagnosis,
minorities (98 percent black) were less likely than whites to receive a complete
examination of the colon (Elston Lafata et al. 2001). The actual rate of
surveillance was 55 percent within 18 months, which compares to the 57
percent of whites receiving posttreatment surveillance within that period of
time in our study. Although the association between posttreatment bowel
surveillance and race in the managed care population did not achieve
statistical signiﬁcance, the magnitude of the difference was similar to what we
observed in a large population of colorectal cancer patients diagnosed over an
Colorectal cancer survival is lower for blacks than for whites and this
may be due, in part, to lower rates of posttreatment endoscopic surveillance.
Although the survival beneﬁt of routine posttreatment bowel surveillance with
colonoscopy and barium enema is unknown, evidence-based clinical guide-
lines should improve clinical outcomes and medical practice. Thus, it is
disturbing that racial variation in the receipt of posttreatment bowel
surveillance exists. We know that a statistically signiﬁcant reduction in the
rate of recurrence and improvement in survival exists among individuals
receiving standard adjuvant therapy for stage III colon cancer. Standard
adjuvant radiation has been shown to reduce recurrences for stages II and III
rectal cancers. However, population-based studies have shown that blacks are
less likely than whites to receive these standards of care that have proven
beneﬁts (Sundararajan et al. 2001; Schrag, Cramer et al. 2001; Potosky et al.
2002; Schrag, Gelfand et al. 2001; Neugut et al. 2002). Our results showing a
lower rate of posttreatment bowel surveillance, coupled with studies showing
Racial Differences in the Receipt of Bowel Surveillance 1899
lower rates of adjuvant therapy receipt among blacks, suggest a consistent
pattern of lower-quality care received by blacks following a diagnosis of
colorectal cancer. The combination of routine posttreatment bowel surveil-
lance and adjuvant therapy need to be evaluated for their potential
contribution to the racial disparity in survival.
Results of this study must be interpreted considering data limitations.
First, claims data are generally constructed for administrative rather than for
research purposes. Because there are a limited number of data ﬁelds in claims
data, codes related to complications may have taken precedence over codes
related to comorbidity, leaving some comorbidity unmeasured. This potential
incomplete measurement of comorbidity is not likely to adequately explain
the observed racial differences in posttreatment bowel surveillance. Second,
the indication for follow-up surveillance was not readily apparent from these
data. The potential exists that bowel examination in response to symptoms
was included with routine posttreatment bowel surveillance procedures in
these data, in which case the rate of routine posttreatment surveillance would
have been overestimated; however, it is unlikely to explain the differentials in
the receipt of procedures that we observed by racial group.
In this large population-based study of Medicare beneﬁciaries aged 65
and older, we found statistically signiﬁcant racial variations in posttreatment
bowel surveillance receipt that were not explained by measured socio-
demographic, hospital, and clinical characteristics. Future studies are needed
to determine if patient preferences or physician characteristics are related to
racial differences in the receipt of posttreatment procedures. In addition, the
impact of racial disparities in the receipt of standard treatment following
colorectal cancer surgery on the racial disparity in outcomes, including
survival and mortality, requires further study.
The authors would like to thank Drs. Rachel Ballard-Barbash and Robert A.
Hiatt for their thoughtful reviews of earlier versions of the manuscript. We
would also like to thank Ms. Nicola Schussler, Information Management
Services, for compiling the dataset used for analysis. Dr. Ellison was a Cancer
Prevention Fellow in the Division of Cancer Prevention, Ofﬁce of Preventive
Oncology, at the National Cancer Institute when he began this work.
1900 HSR: Health Services Research 38:6, Part II (December 2003)
Allison, P. D. 1995. Survival Analysis Using the SAS
System: A Practical Guide. Cary, NC:
Burns, R. B., K. M. Freund, M. A. Moskowitz, L. Kasten, H. Feldman, and J. B.
McKinlay. 1997. ‘‘Physician Characteristics: Do They Inﬂuence the Evaluation
and Treatment of Breast Cancer in Older Women?’’ American Journal of Medicine
103 (4): 263–9.
Charlson, M. E., P. Pompei, K. L. Ales, and C. R. MacKenzie. 1987. ‘‘A New Method of
Classifying Prognostic Cormorbidity in Longitudinal Studies: Development and
Validation.’’ Journal of Chronic Diseases 40 (5): 373–83.
Cooper, G. S., Z. Yuan, C. S. Landefeld, and A. A. Rimm. 1996. ‘‘Surgery for
Colorectal Cancer: Race-Related Differences in Rates and Survival among
Medicare Beneﬁciaries.’’ American Journal of Public Health 86 (4): 582–6.
Cooper, G. S., Z. Yuan, A. Chak, and A. A. Rimm. 1999. ‘‘Geographic and Patient
Variation among Medicare Beneﬁciaries in the Use of Follow-up Testing after
Surgery for Nonmetastatic Colorectal Carcinoma.’’ Cancer 85 (10): 2124–31.
——————. 2000. ‘‘Patterns of Endoscopic Follow-up after Surgery for Nonmetastatic
Colorectal Cancer.’’ Gastrointestinal Endoscopy 52 (1): 33–8.
Cooper-Patrick, L., J. J. Gallo, J. J. Gonzales, H. T. Vu, N. R. Powe, C. Nelson, and D. E.
Ford. 1999. ‘‘Race, Gender, and Partnership in the Patient–Physician Relation-
ship.’’ Journal of the American Medical Association 282 (6): 583–9.
Decosse, J. J., G. J. Tsioulias, and J. S. Jacobson. 1994. ‘‘Colorectal Cancer:
Detection, Treatment, and Rehabilitation.’’ CA: A Cancer Journal for Clinicians
44 (1): 27–42.
Desch, C. E., A. B. Benson III, T. J. Smith, P. J. Flynn, C. Krause, C. L. Loprinz, B. D.
Minsky, N. J. Petrelli, D. G. Pﬁster, and M. R. Somerﬁeld. 1999. ‘‘Recommended
Colorectal Cancer Surveillance Guidelines by the American Society of Clinical
Oncology.’’ Journal of Clinical Oncology 17 (4): 1312–21.
Deyo, R. A., D. C. Cherkin, and M. A. Ciol. 1992. ‘‘Adapting a Clinical Comorbidity
Index for Use with ICD-9-CM Administrative Databases.’’ Journal of Clinical
Epidemiology 45 (6): 613–9.
Elston Lafata, J., C. C. Johnson, T. Ben-Menachem, and R. J. Morlock. 2001.
‘‘Socioeconomic Differences in the Receipt of Colorectal Cancer Surveillance
Care Following Treatment with Curative Intent.’’ Medical Care 39 (4): 361–72.
Fleischer, D. E., S. B. Goldberg, T. H. Browning, J. N. Cooper, E. Friedman, F. H.
Goldner, E. B. Keeffe, and L. E. Smith. 1989. ‘‘Detection and Surveillance of
Colorectal Cancer.’’ Journal of the American Medical Association 261 (4): 580–5.
Goldberg, R. M., T. R. Fleming, C. M. Tangen, C. G. Moertel, J. S. MacDonald, D. G.
Haller, and J. A. Laurie. 1998. ‘‘Surgery for Recurrent Colon Cancer: Strategies
for Identifying Respectable Recurrence and Success Rates after Resection.’’
Annals of Internal Medicine 129: 27–35.
Gornick, M. E. 2000. ‘‘Disparities in Medicare Services: Potential Causes,
Plausible Explanations, and Recommendations.’’ Health Care Financing Review
21 (4): 23–43.
Racial Differences in the Receipt of Bowel Surveillance 1901
Institute of Medicine. 2002. Unequal Treatment: Confronting Racial and Ethnic Disparities
in Health Care, edited by B. D. Smedley, A. Y. Stith, and A. R. Nelson.
Washington, DC: National Academy Press.
Jemal, A., A. Thomas, T. Murray, and M. Thun. 2002. ‘‘Cancer Statistics.’’ CA: A Cancer
Journal for Clinicians 52 (1): 23–47.
Jencks, S. F., T. Cuerdon, D. R. Burwen, B. Fleming, P. M. Houck, A. E. Kussmaul, D.
S. Nilasena, D. L. Ordin, and D. R. Arday. 2000. ‘‘Quality of Medical Care
Delivered to Medicare Beneﬁciaries: A Proﬁle at State and National Levels.’’
Journal of the American Medical Association 284 (13): 1670–6.
Knopf, K. B., J. L. Warren, E. J. Feuer, and M. L. Brown. 2001. ‘‘Bowel Surveillance
Patterns Following a Diagnosis of Colorectal Cancer in Medicare Beneﬁciaries.’’
Gastrointestinal Endoscopy 54 (5): 563–71.
LaVeist, T. A., and T. Carroll. 2002. ‘‘Race of Physician and Satisfaction with Care
among African-American Patients.’’ Journal of the National Medical Association 94
LaVeist, T. A., and A. Nuru-Jeter. 2002. ‘‘Is Doctor-Patient Race Concordance
Associated with Greater Satisfaction with Care?’’ Journal of Health and Social
Behavior 43 (3): 296–306.
Lee, A. J., S. Gehlbach, D. Hosmer, and M. Reti. 1997. ‘‘Medicare Treatment
Differences for Blacks and Whites.’’ Medical Care 35 (12): 1173–89.
McMahon, L. F. Jr., R. A. Wolfe, S. Huang, P. Tedeschi, W. Manning Jr. and M. J.
Edlund. 1999. ‘‘Racial and Gender Variation in Use of Diagnostic Colonic
Procedures in the Michigan Medicare Population.’’ Medical Care 37 (7): 712–7.
Mayberry, R. M., R. J. Coates, H. A. Hill, L. A. Click, V. W. Chen, D. F. Austin, C. K.
Redmond, C. M. Fenoglio-Preister, C. P. Hunter, and M. A. Haynes. 1995.
‘‘Determinants of Black/White Differences in Colon Cancer Survival.’’ Journal of
the National Cancer Institute 87 (22): 1686–93.
Mayberry, R. M., F. Mili, and E. Oﬁli. 2000. ‘‘Racial and Ethnic Differences in Access
to Medical Care.’’ Medical Care Research and Review 57 (supplement, 1): 108–45.
Neugut, A. I., A. T. Fleischauer, V. Sundararajan, N. Mitra, D. F. Heitjan, J. S.
Jacobson, and V. R. Grann. 2002. ‘‘Use of Adjuvant Chemotherapy and
Radiation Therapy for Rectal Cancer among the Elderly: A Population-Based
Study.’’ Journal Clinical Oncology 20 (11): 2643–50.
Potosky, A. L., L. C. Harlan, R. S. Kaplan, K. A. Johnson, and C. F. Lynch. 2002. ‘‘Age,
Sex, and Racial Differences in the Use of Standard Adjuvant Therapy for
Colorectal Cancer.’’ Journal of Clinical Oncology 20 (5): 1192–202.
Ries L. A. G., M. P. Eisner, C. L. Kosary, B. F. Hankey, B. A. Miller, L. Clegg, and B. K.
Edwards, eds. 2002. SEER Cancer Statistics Review, 1973–1999, National Cancer
Institute. Bethesda, MD. Available at http://seer.cancer.gov/csr/1973_1999/.
Rosen, M., L. Chan, R. W. Beart Jr. P. Vukasin, and G. Anthone. 1998. ‘‘Follow-up of
Colorectal Cancer. A Meta-Analysis.’’ Diseases of the Colon and Rectum 41 (9):
SAS Institute. 2001. SAS statistical software (version 8.2). Cary, NC: SAS Institute.
Schapira, M. M., T. L. McAuliffe, and A. B. Nattinger. 2000. ‘‘Underutilization of
Mammography in Older Breast Cancer Survivors.’’ Medical Care 38 (3): 281–9.
1902 HSR: Health Services Research 38:6, Part II (December 2003)
Schrag, D., L. D. Cramer, P. B. Bach, and C. B. Begg. 2001. ‘‘Age and Adjuvant
Chemotherapy Use after Surgery for Stage III Colon Cancer.’’ Journal of the
National Cancer Institute 93 (11): 850–7.
Schrag, D., S. E. Gelfand, P. B. Bach, J. Guillem, B. D. Minsky, and C. B. Begg. 2001.
‘‘Who Gets Adjuvant Treatment for Stage II and III Rectal Cancer? Insight from
Surveillance, Epidemiology, and End Results-Medicare.’’ Journal Clinical
Oncology 19 (17): 3712–18.
Schrag, D., L. J. Hsieh, F. Rabbani, P. B. Bach, H. Herr, and C. B. Begg. 2003.
‘‘Adherence to Surveillance among Patients with Superﬁcial Bladder Cancer.’’
Journal of the National Cancer Institute 95 (8): 588–97.
Sedlis, S. P., V. J. Fisher, D. Tice, R. Esposito, L. Madmon, and E. H. Steinberg. 1997.
‘‘Racial Differences in Performance of Invasive Cardiac Procedures in a
Department of Veterans Affairs Medical Center.’’ Journal of Clinical Epidemiology
50 (8): 899–901.
Shavers, V. L., and M. L. Brown. 2002. ‘‘Racial and Ethnic Disparities in the Receipt of
Cancer Treatment.’’ Journal of the National Cancer Institute 94 (5): 334–57.
Shureiqi, I., C. D. Cooksley, J. Morris, A. S. Soliman, B. Levin, and S. M. Lippman.
2001. ‘‘Effect of Age on Risk of Second Primary Colorectal Cancer.’’ Journal of the
National Cancer Institute 93 (16): 1264–6.
Sundararajan, V., V. R. Grann, J. S. Jacobson, H. Ahsan, and A. I. Neugut. 2001.
‘‘Variations in the Use of Adjuvant Chemotherapy for Node-Positive Colon
Cancer in the Elderly: A Population-Based Study.’’ Cancer Journal 7 (3): 213–8.
Super, N. 2002. ‘‘Medigap: Prevalence, Premiums, and Opportunities for Reform.’’
National Health Policy Forum Issue Brief 782: 1–23.
Vernava, III. A. M., W. E. Longo, K. S. Virgo, M. A. Coplin, T. P. Wade, and F. E.
Johnson. 1994. ‘‘Current Follow-Up Strategies after Resection of Colon Cancer:
Results of a Survey of Members of the American Society of Colon and Rectal
Surgeons.’’ Diseases of the Colon and Rectum 37 (6): 573–83.
Virgo, K. S., A. M. Vernava, W. E. Longo, L. W. McKirgan, and F. E. Johnson. 1995.
‘‘Cost of Patient Follow-up after Potentially Curative Colorectal Cancer
Treatment.’’ Journal of the American Medical Association 273 (23): 1837–41.
Virgo, K. S., T. P. Wade, W. E. Longo, M. A. Coplin, A. M. Vernava III, and F. E.
Johnson. 1995. ‘‘Surveillance after Curative Colon Cancer Resection: Practice
Patterns of Surgical Subspecialists.’’ Annals of Surgical Oncology 2 (6): 472–82.
Warren, J. L., C. N. Klabunde, D. Schrag, P. B. Bach, and G. F. Riley. 2002. ‘‘Overview
of the SEER-Medicare Data: Content, Research Applications and General-
izability to the U.S. Elderly.’’ Medical Care 40 (8 supplement): iv-3–18.
Winawer, S. J., E. T. Stewart, A. G. Zauber, J. H. Bond, H. Ansel, J. D. Waye, D. Hall, J.
A. Hamlin, M. Schapiro, M. J. O’Brien, S. S. Sternberg, and L. S. Gottlieb. 2000.
‘‘A Comparison of Colonoscopy and Double-Contrast Barium Enema
for Surveillance after Polypectomy.’’ New England Journal of Medicine 342 (24):
Racial Differences in the Receipt of Bowel Surveillance 1903