Neighborhood Socioeconomic Status and Use of Colonoscopy in an Insured Population – A Retrospective Cohort Study

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DOI: 10.1371/journal.pone.0036392 · Source: PubMed
Abstract
Low-socioeconomic status (SES) is associated with a higher colorectal cancer (CRC) incidence and mortality. Screening with colonoscopy, the most commonly used test in the US, has been shown to reduce the risk of death from CRC. This study examined if, among insured persons receiving care in integrated healthcare delivery systems, differences exist in colonoscopy use according to neighborhood SES. We assembled a retrospective cohort of 100,566 men and women, 50-74 years old, who had been enrolled in one of three US health plans for ≥1 year on January 1, 2000. Subjects were followed until the date of first colonoscopy, date of disenrollment from the health plan, or December 31, 2007, whichever occurred first. We obtained data on colonoscopy use from administrative records. We defined screening colonoscopy as an examination that was not preceded by gastrointestinal conditions in the prior 6-month period. Neighborhood SES was measured using the percentage of households in each subject's census-tract with an income below 1999 federal poverty levels based on 2000 US census data. Analyses, adjusted for demographics and comorbidity index, were performed using Weibull regression models. The average age of the cohort was 60 years and 52.7% were female. During 449,738 person-years of follow-up, fewer subjects in the lowest SES quartile (Q1) compared to the highest quartile (Q4) had any colonoscopy (26.7% vs. 37.1%) or a screening colonoscopy (7.6% vs. 13.3%). In regression analyses, compared to Q4, subjects in Q1 were 16% (adjusted HR = 0.84, 95% CI: 0.80-0.88) less likely to undergo any colonoscopy and 30%(adjusted HR = 0.70, CI: 0.65-0.75) less likely to undergo a screening colonoscopy. People in lower-SES neighborhoods are less likely to undergo a colonoscopy, even among insured subjects receiving care in integrated healthcare systems. Removing health insurance barriers alone is unlikely to eliminate disparities in colonoscopy use.

Figures

Neighborhood Socioeconomic Status and Use of
Colonoscopy in an Insured Population A Retrospective
Cohort Study
Chyke A. Doubeni
1,2
*, Guruprasad D. Jambaulikar
1
, Hassan Fouayzi
2
, Scott B. Robinson
3
,
Margaret J. Gunter
4
, Terry S. Field
2
, Douglas W. Roblin
5
, Robert H. Fletcher
6
1 Department of Family Medicine and Community Health, Medic al School, University of Massachusetts, Worcester, Massachusetts, United States of America, 2 Meyers
Primary Care Institute/Reliant Medical Group/Fallon Community Health Plan, Department of Medicine, Medical School, University of Massachusetts, Worcester,
Massachusetts, United States of America, 3 Premier Inc., Charlotte, North Carolina, United States of America, 4 LCF Research, Albuquerque, New Mexico, United States of
America, 5 The Center for Health Research-Southeast, Kaiser Permanente Georgia, Atlanta, Georgia, United States of America, 6 Department of Population Medicine,
Harvard Medical School, Boston, Massachusetts, United States of America
Abstract
Background:
Low-socioeconomic status (SES) is associated with a higher colorectal cancer (CRC) incidence and mortality.
Screening with colonoscopy, the most commonly used test in the US, has been shown to reduce the risk of death from CRC.
This study examined if, among insured persons receiving care in integrated healthcare delivery systems, differences exist in
colonoscopy use according to neighborhood SES.
Methods:
We assembled a retrospective cohort of 100,566 men and women, 50–74 years old, who had been enrolled in one
of three US health plans for $1 year on January 1, 2000. Subjects were followed until the date of first colonoscopy, date of
disenrollment from the health plan, or December 31, 2007, whichever occurred first. We obtained data on colonoscopy use
from administrative records. We defined screening colonoscopy as an examination that was not preceded by
gastrointestinal conditions in the prior 6-month period. Neighborhood SES was measured using the percentage of
households in each subject’s census-tract with an income below 1999 federal poverty levels based on 2000 US census data.
Analyses, adjusted for demographics and comorbidity index, were performed using Weibull regression models.
Results:
The average age of the cohort was 60 years and 52.7% were female. During 449,738 person-years of follow-up,
fewer subjects in the lowest SES quartile (Q1) compared to the highest quartile (Q4) had any colonoscopy (26.7% vs. 37.1%)
or a screening colonoscopy (7.6% vs. 13.3%). In regression analyses, compared to Q4, subjects in Q1 were 16% (adjusted
HR = 0.84, 95% CI: 0.80–0.88) less likely to undergo any colonoscopy and 30%(adjusted HR = 0.70, CI: 0.65–0.75) less likely to
undergo a screening colonoscopy.
Conclusion:
People in lower-SES neighborhoods are less likely to undergo a colonoscopy, even among insured subjects
receiving care in integrated healthcare systems. Removing health insurance barriers alone is unlikely to eliminate disparities
in colonoscopy use.
Citation: Doubeni CA, Jambaulikar GD, Fouayzi H, Robinson SB, Gunter MJ, et al. (2012) Neighborhood Socioeconomic Status and Use of Colonoscopy in an
Insured Population A Retrospective Cohort Study. PLoS ONE 7(5): e36392. doi:10.1371/journal.pone.0036392
Editor: Olga Y. Gorlova, The University of Texas M. D. Anderson Cancer Center, United States of America
Received December 12, 2011; Accepted April 5, 2012; Published May 2, 2012
Copyright: ß 2012 Doubeni et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits
unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Funding: This research was supported by the Health Maintenance Organization Cancer Research Network through funding from the National Institutes of
Health/National Cancer Institute (U19CA79689: Cancer Research Network Across Health Care Systems). Dr. Doubeni and Dr. Jambaulikar were also supported by
the National Institutes of Health/National Cancer Institute (5K01CA127118, U54CA163262). The views expressed herein are solely those of the authors and do not
necessarily reflect those of the participating health plans or the Health Maintenance Organization Cancer Research Network or its affiliated entities. The funders
had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have read the journal’s policy and would like to make the following declaration related to employment: Dr. Robinson is
currently employed at Premier, Inc. However, he was employed at LCF Research, Lovelace Health System, Albuquerque, New Mexico at the time the study was
conducted. His affiliation with Premier, Inc. had no impact on the interpretation of the findings of the authors’ study. Hence, this affiliation does not alter the
authors’ adherence to all the PLoS ONE policies on sharing data and materials.
* E-mail: chyke.doubeni@umassmed.edu
Introduction
In the United States, people in low socioeconomic status are
more likely than those from higher socioeconomic groups to be
diagnosed with, and die from, colorectal cancer [1–5]. Screening
with tests such as colonoscopy that are recommended by national
groups in the United States has been shown to reduce the risk of
incidence of or death from colorectal cancer [6–11]. People from
low socioeconomic groups are less likely to undergo colorectal
cancer screening [12–17]. This suggests that socioeconomic
disparities in death from colorectal cancer may result, in part,
from unequal access to and/or unequal use of screening.
Consequently, some public health programs aimed at eliminating
PLoS ONE | www.plosone.org 1 May 2012 | Volume 7 | Issue 5 | e36392
disparities in death from colorectal cancer have focused on
providing greater access to screening [18].
Although observational studies and clinical trials on the efficacy
of colonoscopy are ongoing [19], direct and indirect evidence
including studies in high risk populations support its current use
[7,8,20]. Colonoscopy affords the endoscopist direct visualization
of the entire colon from the rectum to the cecum while making it
possible to remove most precancerous lesions and some early
cancers found at the time of screening [21]. Colonoscopy is also
the recommended diagnostic test in patients with positive findings
on other screening tests [22]. As a result of these appealing
properties, some groups believe and promote colonoscopy as the
best screening test for colorectal cancer [21]. Colonoscopy is now
the most commonly used colorectal cancer screening test in the
United States [12–14], and its use is also increasing in other
countries [23].
Colonoscopy is also the most expensive and invasive of the tests
currently recommended by the US Preventive Services Task Force
[24]. It is not surprising therefore that population-based studies
have consistently shown that people in low socioeconomic status
are less likely to undergo colonoscopy when compared to those
from higher socioeconomic groups [14–17]. The socioeconomic
disparity in colonoscopy use is believed to be due, in part, to
differences in health insurance coverage or access to health care
services. That belief is supported by studies showing a consistently
strong association between the type of health insurance coverage
and colonoscopy use, even among people in Medicare for whom
screening colonoscopy has been a covered benefit since 2001
[14,17,25]. Studies have also shown that differences in colonos-
copy use by socioeconomic status, at the individual or area level,
persist even after accounting for type of health insurance coverage
[14,26].
Those findings suggest that providing health insurance coverage
and removing out-of-pocket cost for colonoscopy, as mandated by
the Affordable Care Act [12,27], may not eliminate socioeconomic
disparities in use of colonoscopy in the United States. Colonoscopy
is a complex screening test involving extensive bowel preparation.
Thus, other financial and non-financial barriers to health care for
low-income populations including cultural barriers, the need for
time off work or other competing social needs, and difficulties in
navigating healthcare systems [28], may continue to limit
colonoscopy use for low-income populations. However, it remains
largely unknown whether socioeconomic differences in colonos-
copy use persist when health insurance and out-of-pocket cost
barriers are removed.
Integrated healthcare delivery systems provide an appropriate
setting to evaluate the potential impact of removing out-of-pocket
cost barriers on socioeconomic disparities in colonoscopy use. In
this study, we evaluated whether the use of colonoscopy in
populations with similar health insurance coverage with little or no
out-of-pocket cost and an available usual place of health care
differed according to neighborhood socioeconomic status. Our
study population, unlike Medicare, was comprised mostly of
employed persons who were insured and received care from a
common healthcare provider network.
Methods
Ethics Statement
This study was reviewed by the Institutional Review Boards of
the University of Massachusetts Medical School (Worcester, MA)
and the participating sites. Because the study did not involve
contact with study subjects, it was considered exempt from a full
human subjects review and from obtaining informed consent.
Study Design and Population
This was a cohort study that used electronic administrative and
clinical data for persons who were, on January 1, 2000, members
of Reliant Medical Group/Fallon Community Health Plan in
Massachusetts, Kaiser Permanente Georgia, or Lovelace Health
System in New Mexico. These health care systems are part of the
HMO Cancer Research Network, which currently has fourteen
member organizations that use varying models of health care
delivery. The health plans have programs to promote preventive
healthcare, including periodic reminders on cancer screening. All
subjects were insured and had access to care from a common
clinical provider network at each study site. Colorectal cancer
screening at each site was provided according to prevailing
national recommendations as a covered benefit to the members.
The historical cohort for this study was comprised of men and
women who were between the ages of 50 and 74 years, and had
been members of one of three participating health plans for at least
1 calendar year (1999) as of January 1, 2000. We excluded all
subjects who had a diagnosis of colorectal cancer using a broad
definition of one record, or more, of any International Classifi-
cation of Disease, 9
th
Edition, Clinical Modification (ICD9) code
for colorectal cancer in the 1999 calendar year period in the
clinical databases of the health plan. We then tracked the
utilization history of the subjects until they received their first
colonoscopy, the last date of known enrollment in the health plan,
or the end of the study period (December 31, 2007), whichever
occurred first.
Data on Use of Colonoscopy
Data, including dates, on medical diagnoses and procedures
received by subjects were obtained from the electronic adminis-
trative and clinical databases using ICD9, Common Procedure
Terminology (CPT) and Healthcare Common Procedure Coding
System (HCPCS) codes. The use of colonoscopy was identified
using the following codes: ICD9 45.23, 45.25, 45.42, 45.43; CPT
44388–9, 44392–4, 45378, 45380, 45382, 45383–45385, 45388;
and HCPCS G0105 and G0121. We also created a variable for
screening colonoscopy use, which was defined as a colonoscopy
that was not preceded by a gastrointestinal condition in the prior 6
months, using an approach like that described by Ko et al. [29].
The presence of gastrointestinal conditions was based on a record
of any of the following ICD9 codes in electronic data:
gastrointestinal bleeding (456.0, 456.20, 530.82, 531.xx-534.xx,
535.01–535.41, 535.51, 535.61, 562.02, 562.03, 562.12, 562.13,
578.0, 578.1, or 578.9), occult bleeding (792.1), anemia (280 or
285.9), abdominal pain (787.3, 789.0 or 789.6), weight loss (783.2),
inflammatory bowel disease (555.xx-556.xx, 558.2 or 558.9), or
history of colon polyps (V12.72, 211.3, or 211.4).
Data on Neighborhood Socioeconomic Status
We obtained data on socioeconomic factors on each subject
through linkage of residential addresses to 2000 US decennial
census data at the census-tract level of aggregation. For this study,
we used the percentage of households in the census tract with
incomes below the 1999 federal poverty level as our measure of
neighborhood socioeconomic status. This measure was highly
correlated (r = 0.97, p-value,0.001) with a summary index of
neighborhood socioeconomic deprivation derived by performing
principal factor analyses on 19 census variables as described in
previous publications [30,31]. The cohort was divided into
quartiles based on household poverty levels, such that subjects in
census-tracts with the highest levels of household poverty (or
lowest socioeconomic status) in the study comprised quartile 1 and
Health Insurance, SES and Use of Colonoscopy
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census-tracts in the highest socioeconomic group comprised
quartile 4.
Data on Covariates
We also obtained electronic data on subjects’ age, sex, race
(whites, blacks, others, or missing), and length of health plan
enrollment. The Deyo modification of the Charlson comorbidity
index (categorized as 0, 1, and 2+) was calculated using the data on
medical diagnoses and procedures during the 1999–2000 calendar
years period [32].
Statistical Analysis
We compared the characteristics of the cohort according to
quartiles of neighborhood socioeconomic status using the Chi-
square test for categorical variables and analysis of variance test for
continuous variables. We used parametric survival models with
Weibull distribution and gamma frailties to estimate the associ-
ation between quartiles of neighborhood socioeconomic status
(census-tract household poverty level) and use of any colonoscopy
or screening colonoscopy during the 8-year follow-up period.
Frailty models allowed us to evaluate geographic variability in
colonoscopy use across census-tracts with the likelihood ratio test.
We also accounted for clustering of subjects within census-tracts in
the analyses. Multivariate analyses adjusted for age at baseline,
sex, modified Charlson comorbidity index, study site (health plan),
and length of health plan enrollment. We also conducted analyses
stratified by health plan and age (50–64 vs. 65–74 years). The age
cutoff for the stratified analyses was based on the Medicare age
eligibility criterion. About 50% of the subjects in the fourth
quartile and 73% in the first quartile had missing data on race.
Therefore, we did not include race or ethnicity in our estimation
models. All analyses were performed using STATA version 12.1
(StataCorp 2011. College Station, TX: StataCorp LP).
Results
There was a total of 100,566 subjects from the three health
plans in 1,536 census-tracts analyzed for this study, of whom
53,042 (52.7%) were female, the average age was 60 (range 50–74)
years and 69,286 (68.9%) were younger than 65 years of age. The
mean follow-up on the study was 4.5 years. Table 1 shows the
characteristics of cohort by quartiles of neighborhood socioeco-
nomic status (SES). Subjects in low-SES (higher poverty) areas
were older and more likely to be female. The length of enrollment
in the health plans also varied across SES quartiles: 9,906 (39.7%)
subjects in the first (lowest SES) quartile remained enrolled in the
health plan for the full 8 years of follow-up on the study compared
to 12,562 (48.4%) in the fourth (highest SES) quartile.
During 449,738 person-years of follow-up on the study, 33,630
(33.4%) subjects had at least 1 colonoscopy including 11,093
(11.0%) screening colonoscopies. Table 2 compares the use of any
colonoscopy by neighborhood SES. Compared to the fourth
quartile (n = 9,617; 37.1%), fewer subjects in the second
(n = 7,859; 32.1%) or first (n = 6,658; 26.7%) SES quartile had
any colonoscopy. Table 2 also shows the results of Weibull
regression models analyses on the association between neighbor-
hood SES and any colonoscopy use. Compared to subjects in the
fourth quartile, subjects’ likelihood of colonoscopy use decreased
with decreasing neighborhood SES. In the unadjusted model,
those in the first quartile were about 19% (hazard ratio
[HR] = 0.81, 95% confidence interval [CI]: 0.77–0.86) less likely
to have had any colonoscopy than subjects in the fourth quartile.
The association between SES and colonoscopy use was stable
(HR = 0.84, 95% CI: 0.80–0.88) to adjustment for age, gender,
study site, modified Charlson comorbidity index, and number of
years of enrollment. The use of colonoscopy also varied across the
census-tracts in the study (likelihood ratio test p-value,0.001).
Tables 3 compares the use of screening colonoscopy across
SES quartiles. Fewer subjects in the first quartile (n = 1,908; 7.6%)
or second (n = 2,463; 10.1%) than in the fourth quartile (n = 3,447;
13.3%) had a screening colonoscopy during the follow-up period.
In unadjusted Weibull regression analyses, subjects in the first
quartile were about 34% (HR = 0.66, 95% CI: 0.61–0.72) less
likely to have had a screening colonoscopy compared to those in
the fourth quartile. In the adjusted analyses, compared to the
fourth quartile, subjects in the first quartile were about 30%
(HR = 0.70, 95% CI: 0.65–0.75) less likely to have had a screening
exam. Similar to analysis on any colonoscopy, there was
statistically significant heterogeneity in the use of screening
colonoscopy across the census-tracts (likelihood ratio test p-
value,0.001).
Table 4 shows analyses on the association between neighbor-
hood SES and colonoscopy use stratified by age and study sites
(health plan). In the adjusted analyses among subjects 50–64 years
of age (n = 69,286), compared to the fourth quartile, subjects in the
first quartile were about 17% (HR = 0.83, 95% CI: 0.78–0.87) less
likely to have any colonoscopy and 30% (HR = 0.70, 95% CI:
0.65–0.76) less likely to have had a screening exam. The findings
were similar from analysis on subjects 65–74 years of age
(n = 31,280) for any colonoscopy (HR = 0.88, 95% CI: 0.83–
0.93) or screening colonoscopy (HR = 0.71, 95% CI: 0.63–0.80).
We also found similar results across the 3 health plans:
neighborhood SES was significantly associated with colonoscopy
use in a dose response fashion irrespective of the health plan
analyzed.
Discussion
In this study, we examined the association between neighbor-
hood socioeconomic status (defined by percent of households
below the federal poverty level) and use of colonoscopy in an
insured population. A unique characteristic of the population was
that, within each study site, subjects were in the same health plan
and served by the same clinical provider network, and thus the
ability to acess a usual place of care. The health systems included
in this study provide colonoscopy as a covered benefit to members
and also had systems to encourage members to use preventive
health services. These characteristics of the healthcare environ-
ment would be expected to mitigate barriers to the use of
colonoscopy for persons in low-socioeconomic status and thus
lessen disparities.
We found significant socioeconomic differences in the use of
colonoscopy. Persons residing in the lowest SES neighborhoods
were 16% less likely to undergo any colonoscopy relative to those
in the highest SES neighborhoods. This association was even
stronger (30%) when only screening colonoscopy was considered.
Socioeconomic differences in colonoscopy use observed in the
general population could be attributed to the fact that people
receive care from diverse clinical provider networks and have
differing types of health insurance coverage [12–17]. However,
our results suggest that simply having health insurance and a usual
place of care are not enough to eliminate socioeconomic disparities
in the use of colonoscopy use, and that other factors related to
poverty limit or restrict colonoscopy use. Elimination of disparities
concerning colorectal cancer for socioeconomically disadvantaged
populations will require measures that also address other
economic, social and cultural barriers to receipt of health care
services.
Health Insurance, SES and Use of Colonoscopy
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Our findings, together with existing research, suggest the need
for effective patient navigation or outreach programs in integrated
healthcare delivery systems to address disparities in colonoscopy
use. Also, performance incentives based on Healthcare Effective-
ness Data and Information Set (HEDIS) measures, as practiced in
some health care systems, could be effective means to address the
disparities we found [33]. However, the effectiveness of such
programs in eliminating socioeconomic disparities in colonoscopy
use among people receiving their health care under the auspices of
healthcare delivery systems is unproven and needs to be studied.
There are few published studies on area-level variations in the
use of colonoscopy; very few, if any, of such studies have been
conducted within integrated healthcare delivery system settings.
Our findings, however, are consistent with studies on Medicare
populations showing disparities based on individual-level measures
of socioeconomic status [14,17]. Klabunde et al., using 2008 US
National Health Interview Survey data, found that about 34% of
screening-eligible adults in families at #200% of federal poverty
level had colonoscopy compared to 58% among those at $500%
of federal poverty level, a 1.7-fold difference [13]. A study using
Missouri Behavioral Risk Factor Surveillance Survey data also
reported that the use of colorectal cancer screening varied across
zip-code areas as well as by zip-code poverty levels; socioeconomic
differences remained even after adjustment for health insurance
Table 1. Characteristics of the study cohort according to neighborhood socioeconomic status, N = 100,566.
Quartiles of neighborhood socioeconomic status*
Characteristics, n (%)
Quartile 1 N = 24,959 Quartile 2 N = 24,503 Quartile 3 N = 25,148 Quartile 4 N = 25,956
Age, years
50–54 7523 (30.1) 7353 (30.0) 7804 (31.0) 8735 (33.7)
55–59 5364 (21.5) 5234 (21.4) 5289 (21.0) 5875 (22.6)
60–64 4170 (16.7) 3956 (16.1) 3937 (15.7) 4046 (15.6)
65–69 4188 (16.8) 4249 (17.3) 4418 (17.6) 4056 (15.6)
70–74 3714 (14.9) 3711 (15.1) 3700 (14.7) 3244 (12.5)
Female 13503 (54.1) 13054 (53.3) 13262 (52.7) 13223 (50.9)
Study site/Health plan
A 5150 (20.6) 8298 (33.9) 12031 (47.8) 9904 (38.2)
B 4652 (18.6) 5887 (24.0) 7183 (28.6) 9567 (36.9)
C 15157 (60.7) 10318 (42.1) 5934 (23.6) 6485 (25.0)
Enrollment history
Percent enrolled at year 5 12844 (51.5) 14503 (59.2) 16562 (65.9) 16707 (64.4)
Percent enrolled at year 8 9906 (39.7) 11090 (45.3) 12701 (50.5) 12562 (48.4)
Modified Charlson comorbidity Index at
baseline
0 21435 (85.9) 20097 (82.0) 19489 (77.5) 21433 (82.6)
1 1801 (7.2) 2249 (9.2) 2949 (11.7) 2410 (9.3)
2+ 1723 (6.9) 2157 (8.8) 2710 (10.8) 2113 (8.1)
Note: The p-value statistic for heterogeneity across categories was ,0.001 on all variable s.
*Neighborhood socioeconomic status was measured by the percentage of households in the census-tract level below the 1999 federal poverty levels based on 2000 US
census. Quartile 1 corresponds to the lowest socioeconomic (highest household poverty rates) group and Quartile 4 corresponds to the census tracts with the highest
socioeconomic status relative to others in the study.
doi:10.1371/journal.pone.0036392.t001
Table 2. Association between neighborhood socioeconomic status and use of any colonoscopy, 2000–2007.
Quartiles of neighborhood socioeconomic status* Colonoscopies, n (%)
Hazard ratio (95% confidence interval)
Unadjusted Adjusted{
1st quartile 6658 (26.7) 0.81 (0.77–0.86) 0.84 (0.80–0.88)
2nd quartile 7859 (32.1) 0.89 (0.84–0.94) 0.89 (0.86–0.93)
3rd quartile 9496 (37.8) 0.99 (0.94–1.04) 0.97 (0.93–1.01)
4th quartile 9617 (37.1) 1.00 1.00
*Neighborhood socioeconomic status was measured by the percentage of households in the census-tract level below the 1999 federal poverty levels based on 2000 US
census. Quartile 1 corresponds to the lowest socioeconomic (highest household poverty rates) group and Quartile 4 corresponds to the census tracts with the highest
socioeconomic status relative to others in the study.
{
Estimates were adjusted for age at baseline, gender, modified Charlson comorbidity index at baseline, number of years of enrollment and health plan. Likelihood-ratio
test p-value for heterogeneity across census tract was ,0.001.
doi:10.1371/journal.pone.0036392.t002
Health Insurance, SES and Use of Colonoscopy
PLoS ONE | www.plosone.org 4 May 2012 | Volume 7 | Issue 5 | e36392
type and having a primary care provider [26]. Our study
examined socioeconomic differences in colonoscopy use in a
smaller area of aggregation and found both geographic and
socioeconomic variations.
The population we studied was comprised predominantly of
employed persons from varying socioeconomic backgrounds.
Socioeconomic status is a predictor of both where people live
and colorectal cancer testing. Therefore, the findings from this
study are a reflection of the socioeconomic diversity among the
members of the respective health care systems, which might
influence screening colonoscopy use in several possible ways in
integrated healthcare delivery systems. People from low-socioeco-
nomic groups may be late adopters [34] of colonoscopy which has
been used increasingly for routine screening in recent years, and
they may have greater ambivalence about the balance of risks and
benefits associated with the test. Factors related to poverty such as
resource deprivation as posited in the Deprivation-Amplification
hypothesis [35], cultural barriers, and difficulty navigating
healthcare systems, may act separately or together to restrict
access to colonoscopy [28]. The need for transportation to and
from the procedure may disproportionately impact those from
lower socioeconomic groups, despite having health insurance.
People in low socioeconomic status may also experience a greater
negative impact from the time and preparation required for
colonoscopy and the burden of taking time off from work.
Although the enrollees were insured, the health plans provide a
variety of insurance programs with varying levels of coverage for
colonoscopy. The burden of out-of-pocket expenses may dis-
proportionally impact low-income people in the health plans
studied. The co-pay for colonoscopy in the health plans across all
coverage types during the study period was between $0 and $200.
A study of 106 health plans in the United States found that out-of-
pocket costs of $300 or greater negatively affect colonoscopy use
[36]. This suggests that potential differences in co-pay among
study subjects are unlikely to explain our findings. Further,
analyses stratified on health plan or age confirmed the results.
There may also be socioeconomic differences in the patient-
physician communication [37] around colorectal cancer screening,
Table 3. Association between neighborhood poverty and use of screening colonoscopy, 2000–2007.
Quartiles of neighborhood socioeconomic status* Colonoscopies, n (%)
Hazard ratio (95% confidence interval)
Unadjusted Adjusted{
1st quartile 1908 (7.6) 0.66 (0.61–0.72) 0.70 (0.65–0.75)
2nd quartile 2463 (10.1) 0.79 (0.73–0.86) 0.80 (0.75–0.85)
3rd quartile 3275 (13.0) 0.94 (0.87–1.01) 0.92 (0.86–0.97)
4th quartile 3447 (13.3) 1.00 1.00
*Neighborhood socioeconomic status was measured by the percentage of households in the census-tract level below the 1999 federal poverty levels based on 2000 US
census. Quartile 1 corresponds to the lowest socioeconomic (highest household poverty rates) group and Quartile 4 corresponds to the census tracts with the highest
socioeconomic status relative to others in the study.
{
Estimates were adjusted for age at baseline, gender, modified Charlson comorbidity index at baseline, number of years of enrollment and health plan. Likelihood-ratio
test p-value for heterogeneity across census tract was ,0.001.
doi:10.1371/journal.pone.0036392.t003
Table 4. Association between neighborhood socioeconomic status and use of colonoscopy according to age and health plan,
2000–2007.
Adjusted hazard ratios (95% confidence interval ){
Colonoscopy outcome and quartiles of
neighborhood socioeconomic status*
According to age According to health plan
50–64 years 65–74 years A B C
Any colonoscopy N = 69,286 N = 31,280 N = 35,383 N = 27,289 N = 37,894
1st quartile 0.83 (0.78–0.87) 0.88 (0.83–0.93) 0.82 (0.77–0.87) 0.83 (0.77–0.90) 0.84 (0.77–0.91)
2nd quartile 0.89 (0.84–0.93) 0.92 (0.87–0.98) 0.92 (0.87–0.98) 0.87 (0.81–0.94) 0.90 (0.82–0.99)
3rd quartile 0.95 (0.90–0.99) 1.01 (0.96–1.07) 1.00 (0.95–1.05) 0.94 (0.87–1.01) 0.96 (0.86–1.06)
4th quartile 1.00 1.00 1.00 1.00 1.00
Screening colonoscopy
1st quartile 0.70 (0.65–0.76) 0.71 (0.63–0.80) 0.70 (0.63–0.78) 0.68 (0.59–0.77) 0.71 (0.63–0.81)
2nd quartile 0.80 (0.75–0.87) 0.81 (0.72–0.90) 0.85 (0.77–0.93) 0.74 (0.66–0.84) 0.82 (0.72–0.94)
3rd quartile 0.93 (0.87–0.99) 0.90 (0.81–1.00) 0.99 (0.91–1.07) 0.84 (0.75–0.93) 0.93 (0.81–1.08)
4th quartile 1.00 1.00 1.00 1.00 1.00
*Neighborhood socioeconomic status was measured by the percentage of households in the census-tract level below the 1999 federal poverty levels based on 2000 US
census. Quartile 1 corresponds to the lowest socioeconomic (highest household poverty rates) group and Quartile 4 corresponds to the census tracts with the highest
socioeconomic status relative to others in the study.
{
Estimates were adjusted for age at baseline, gender, modified Charlson comorbidity index at baseline, number of years of enrollment and health plan. Likelihood-ratio
test p-value for heterogeneity across census tract was ,0.001.
doi:10.1371/journal.pone.0036392.t004
Health Insurance, SES and Use of Colonoscopy
PLoS ONE | www.plosone.org 5 May 2012 | Volume 7 | Issue 5 | e36392
including differences in physician recommendation for colonosco-
py, that may account for some of the differences observed. It is also
possible that people of a lower socioeconomic status may
experience higher levels of mistrust of the medical care system
and may have greater difficulties gaining access to health care
systems despite having health insurance [38]. Other barriers may
include embarrassment, lack of knowledge and cultural factors
[39–41]. Analyses of these potential barriers for insured popula-
tions are beyond the scope of our study, but warrant further
investigation.
Although we were not able to determine if our findings were
solely the result of patient, provider or healthcare system factors,
the findings do suggest the need to pay greater attention to the
preventive care needs of all people who reside in socioeconom-
ically deprived neighborhoods regardless of whether or not they
have health insurance. Area-based socioeconomic measures are
readily accessible and can be utilized to guide the implementation
of patient navigator programs and reminder systems [42–44].
Our study has other limitations. We relied on codes in electronic
administrative and clinical databases to ascertain colonoscopy
utilization and did not have precise measurements of screening
colonoscopy. This might have led to a non-differential misclassi-
fication of the outcome, thus attenuating differences. A more
accurate measurement may have found larger socioeconomic
disparities in colonoscopy use.
We did not have individual-level measures of socioeconomic
status determinants such as education, income or occupation.
Therefore, the observed neighborhood effects cannot be inter-
preted as being independent of individual-level socioeconomic
factors. However, given the challenges of collecting information on
individual-level socioeconomic data, our findings reinforce the
value of area-level socioeconomic data as being a suitable
approach for assessing socioeconomic disparities in colorectal
cancer screening. Further, while neighborhood poverty level may
not fully reflect the poverty level of individuals within an area and
its effect on their use of colonoscopy, the contextual factors
captured by neighborhood measures provide information beyond
characteristics of individuals alone. Prior research also shows that
neighborhood socioeconomic measures have similar predictive
power as individual measures [2]. Another limitation was that over
one-half of the subjects had missing data on race. We were
therefore unable to account for potential confounding by race on
the associations studied. However, prior research suggests that
inclusion of race in the analyses would not substantially alter our
results [14,17].
Finally, we did not follow subjects for 10 years, which is the
recommended interval for screening colonoscopy. This may have
resulted in an underestimation of the true socioeconomic effect if
subjects from high-SES neighborhoods had continued to have
higher rates of colonoscopy use past the 8 years of follow-up on
this study.
In conclusion, this study found that, among insured persons
receiving care in integrated health care delivery systems, those
residing in poor neighborhoods were less likely to have had a
colonoscopy compared to persons in high-SES neighborhoods,
despite receiving care from a common clinical provider network.
Therefore, providing health insurance or even free colonoscopy
services, a sound public health policy, may not eliminate
socioeconomic disparities in colonoscopy use without attention
to other barriers. Future studies of financial and non-financial
barriers to colonoscopy use are needed to identify effective
approaches to eliminate disparities in colonoscopy use in insured
populations.
Acknowledgments
We are grateful to the HMO Cancer Research Network, especially the
participating health plans, for their assistance with the study. We are
grateful to Sarah Beaton, PhD, Senior Research Associate at the Lovelace
Clinic Foundation for comments on the revised manuscript and help with
gathering cost-sharing data on the health plans.
Author Contributions
Conceived and designed the experiments: CAD SBR MJG TSF DR RHF.
Performed the experiments: CAD. Analyzed the data: CAD HF GDJ.
Wrote the paper: CAD GDJ HF. Critical review of the manuscript: CAD
SBR MJG TSF DR RHF Project director: CAD.
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Health Insurance, SES and Use of Colonoscopy
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    • "We evaluated adherence to CRCS following current USPSTF guidelines, while others [16,21] evaluated various ways of screening, including CRCS within the previous year regardless of test modality and lifetime use of FOBT. Finally, unlike previous studies [15,21] that employed categorical measures of area-level SES, our study evaluated continuous measures. It is important to highlight that no consensus exists in the cancer screening literature regarding the best way to measure contextual variables [14] although some recommendations have been made [24]. "
    [Show abstract] [Hide abstract] ABSTRACT: Background: Colorectal cancer is the third most commonly diagnosed cancer and the third leading cause of cancer death in the United States. Increased attention has been given to understanding the role of local contexts on cancer screening behaviors. We examined the associations between multiple tract-level socioeconomic measures and adherence to colorectal cancer screening (CRCS) in Harris County and the City of Houston, Texas. Methods: We conducted a cross-sectional multilevel study linking individual-level data on CRCS from the 2010 Health of Houston Survey with contextual data from the U.S. Census and the U.S. Department of Housing and Urban Development. We examined tract-level poverty, education, employment, income inequality, and foreclosure measures across 543 Census tracts. Analyses were limited to individuals aged 50-74 years (N=1720). Results: Overall, 58.0% of the sample was adherent to any recommended CRCS test. In bivariate analyses, increasing levels of area poverty, low education, unemployment, and foreclosures were associated with lower odds of adherence to CRCS. After controlling for individual-level covariates, only tract-level unemployment remained associated with adherence to CRCS (adjusted OR=0.80; 95% CI: 0.66-0.99; P=.037). Conclusions: Neighborhood socioeconomic disadvantage is increasingly recognized as a determinant of health, and our study suggests that the contextual effect of area unemployment may extend to cancer screening outcomes. Our finding is important to cancer control planners because we identified a contextual marker of disparity that can be used to target local interventions to promote CRCS and thereby reduce cancer disparities among non-adherent individuals who reside in communities with high unemployment rates.
    Article · Dec 2015
    • "Audits were standardized through training and retraining and through the use of a common, structured electronic data collection instrument that was developed in Microsoft Access. The data collection tool was pre-populated with patient demographics , health care utilization history and the dates of CRC tests that were extracted from electronic databases using, in part, codes from the International Classification of Diseases, 9 th Edition, Clinical Modification, Current Procedural Terminology and Healthcare Common Procedure Coding System [28]. For each test found in the medical records, the auditors collected up to three documented reasons, separately, from each of three data sources (progress notes, referral note, and procedure report ) according to 28 pre-coded categories (see Additional file 1: Appendix B). "
    [Show abstract] [Hide abstract] ABSTRACT: Accurate indication classification is critical for obtaining unbiased estimates of colonoscopy effectiveness and quality improvement efforts, but there is a dearth of published systematic classification approaches. The objective of this study was to evaluate the effects of data-source and adjudication on indication classification and on estimates of the effectiveness of screening colonoscopy on late-stage colorectal cancer diagnosis risk. This was an observational study in members of four U.S. health plans. Eligible persons (n = 1039) were age 55-85 and had been enrolled for 5 years or longer in their health plans during 2006-2008. Patients were selected based on late-stage colorectal cancer diagnosis in a case-control design; each case patient was matched to 1-2 controls by study site, age, sex, and health plan enrollment duration. Reasons for colonoscopies received in the 10-year period before the reference date were collected from three medical records sources (progress notes; referral notes; procedure reports) and categorized using an algorithm, with committee adjudication of some tests. We evaluated indication classification concordance before and after adjudication and used logistic regressions with the Wald Chi-square test to compare estimates of the effects of screening colonoscopy on late-stage colorectal cancer diagnosis risk for each of our data sources to the adjudicated indication. Classification agreement between each data-source and adjudication was 78.8-94.0% (weighted kappa = 0.53-0.72); the highest agreement (weighted kappa = 0.86-0.88) was when information from all data sources was considered together. The choice of data-source influenced the association between screening colonoscopy and late-stage colorectal cancer diagnosis; estimates based on progress notes were closest to those based on the adjudicated indication (% difference in regression coefficients = 2.4%, p-value = 0.98), as compared to estimates from only referral notes (% difference in coefficients = 34.9%, p-value = 0.12) or procedure reports (% difference in coefficients = 27.4%, p-value = 0.23). There was no single gold-standard source of information in medical records. The estimates of colonoscopy effectiveness from progress notes alone were the closest to estimates using adjudicated indications. Thus, the details in the medical records are necessary for accurate indication classification.
    Full-text · Article · Feb 2014
    • "We found that only about one in three patients followed up in Swiss University primary care settings were screened for CRC. This relatively low CRC screening rate is comparable with those reported in some underserved populations in the USA (Doubeni et al., 2012). We found three characteristics to be associated with lower CRC screening rates: being overweight or obese, male sex of the physician in charge, and being born in a country outside of Western Europe and North America. "
    [Show abstract] [Hide abstract] ABSTRACT: Screening for colorectal cancer (CRC) is associated with reduced CRC mortality, but low screening rates have been reported in several settings. The aim of the study was to assess predictors of low CRC screening in Switzerland. A retrospective cohort of a random sample of 940 patients aged 50-80 years followed for 2 years from four Swiss University primary care settings was used. Patients with illegal residency status and a history of CRC or colorectal polyps were excluded. We abstracted sociodemographic data of patients and physicians, patient health status, and indicators derived from RAND's Quality Assessment Tools from medical charts. We defined CRC screening as colonoscopy in the last 10 years, flexible sigmoidoscopy in the last 5 years, or fecal occult blood testing in the last 2 years. We used bivariate and multivariate logistic regression analyses. Of 940 patients (mean age 63.9 years, 42.7% women), 316 (33.6%) had undergone CRC screening. In multivariate analysis, birthplace in a country outside of Western Europe and North America [odds ratio (OR) 0.65, 95% confidence interval (CI) 0.45-0.97], male sex of the physician in charge (OR 0.67, 95% CI 0.50-0.91), BMI 25.0-29.9 kg/m (OR 0.66, CI 0.46-0.96) and at least 30.0 kg/m (OR 0.61, CI 0.40-0.90) were associated with lower CRC screening rates. Obesity, overweight, birthplace outside of Western Europe and North America, and male sex of the physician in charge were associated with lower CRC screening rates in Swiss University primary care settings. Physician perception of obesity and its impact on their recommendation for CRC screening might be a target for further research.
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