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.
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,
between 1986 and 1996, and were followed through December 31, 1998. Cox
Proportional Hazards modelswereusedto investigate the relationofraceand receiptof
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,
blacks were 25 percent less likely than whites to receive surveillance if diagnosed
between 1991 and 1996 (RR50.75, 95 percent CI50.70–0.81).
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-
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 tumorsoccur at a rate of
0.35percent peryear(Virgoetal.1995),andtherisk ishigheramongyounger
(o65 years) than among older age groups (Shureiqi et al. 2001).
Because patients receiving potentially curative colorectal cancersurgery
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.
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)
alwaysaccountforindividualvariationamong patientsand adherenceisoften
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
disparities over time. As in the case of breast cancer screening, it might be
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 Surveillance1887
siteof the tumor, stage,and histology, as wellas 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 ofindividualsaged65andolderinthe UnitedStates.Medicareclaims
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 withcolorectal cancer beforeage 65, diagnosed by deathcertificate
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
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
by SEER, and patients who developed recurrent colorectal cancer.
We searched the Medicare claims for all bowel surveillance procedures from
the indexdateuntilthedate ofcensoringorDecember31,1998.Weexcluded
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
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 CouncilofTeaching 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
wasassessed using Kaplan-Meier (K-M) curves,and thelog-ranktest wasused
Racial Differences in the Receipt of Bowel Surveillance1889
to investigate statistical differences in posttreatment surveillance between
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,
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
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 (n544,768), black (n52,921),
and members of other racial groups (n54,416) 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
Hispanic whites tended to be older than other groups at diagnosis. A higher
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)
ColorectalCancer Patient Characteristics,SEER-Medicare,
Age at Diagnosisn
Year of Diagnosisn
Geographic Region of Residence
San Francisco/Oakland/San Jose
Percent of Census-tract without High School
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-ranktest,po0.001). Fifty-seven percent ofwhites,48 percent
of blacks, and 45 percent of others received posttreatment surveillance within
American College of Surgeons
Council of Teaching Hospitals
Charlson Comorbidity Score
wPercent 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.
zUnable to calculate Charlson Comorbidity Score for missing records.
zNot statistically significant.
1892HSR: Health Services Research 38:6, Part II (December 2003)
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
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 (p50.008). 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 (RR50.87, 95 percent CI50.80–0.94; RR50.91, 95 percent
CI50.84–1.00 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 (RR50.75, 95 percent
CI50.70–0.81). No statistically significant differences in posttreatment bowel
0 20 4060 80100120140 160
Months Since Index Date
Chance of Surveillance
Potentially Curative Surgery, SEER-Medicare: 1986–1998
Time to Receipt of a First Bowel Surveillance Procedure Following
Racial Differences in the Receipt of Bowel Surveillance1893
Adjusted Cox Proportional Hazards Models for Time to First Bowel Surveillance Following Potentially
Curative Surgery, SEER-Medicare: 1986–1998
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)
AdjustednProbability 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
nAdjusted 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
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 (OR51.39, 95 percent
CI51.18–1.63). 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, p50.02) 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 surveillanceprocedure (RR50.91;
CI50.85–0.98). 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,
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
these differences have been noted, the reasons for these differences are not
well understood. These differences may be the result of problems with access
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
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 Surveillance1897
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 differencesinthereceiptofbowelsurveillance.We wereunable
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
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
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 theuse 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 Download full-text
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
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,
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 overan
Colorectal cancer survival is lower for blacks than for whites and this
may be due, in part, to lower rates of posttreatment endoscopic surveillance.
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 Surveillance1899