Correlates of screening sigmoidoscopy use among men in a large nonprofit health plan
As the majority of patients diagnosed with colorectal cancer have no known risk factors, regular screening is strongly recommended. The authors examined factors associated with screening sigmoidoscopy use among participants in the California Men's Health Study (CMHS).
The authors conducted a cross-sectional study over a 5-year period nested within a prospective cohort study. The CMHS enrolled a large multiethnic cohort (n = 84,170) of men from 2 major California health plans. Because screening sigmoidoscopy was the preferred and most commonly used test for patients at average risk of colorectal cancer in the health plans, the authors excluded from the analysis men who completed a barium enema colonoscopy or a fecal occult blood test.
Eligible subjects included 39,559 men at average risk for colorectal cancer. Prevalence of screening sigmoidoscopy use decreased with older age and increased with higher education and household income over the 5-year study period. Compared with whites, Asians (adjusted OR, 1.42; 95% CI, 1.30–1.56) and African Americans (adjusted OR, 1.18; 95% CI, 1.08–1.29) were more likely to undergo screening sigmoidoscopy. Screening increased with the number of outpatient visits and with having a primary care provider in internal medicine. Men who did not undergo prostate-specific antigen testing were also less likely to undergo sigmoidoscopy screening. Only 24.5% of current smokers had a screening sigmoidoscopy examination and were 25% less likely to undergo this procedure compared with nonsmokers (adjusted OR, 0.75; 95% CI, 0.69–0.82).
In this insured population for whom financial barriers are minimized, screening sigmoidoscopy use was as low as reported in the general population. However, minority patients were not less likely to be screened. Cancer 2007. © 2007 American Cancer Society.
Colorectal cancer (CRC) is the third most common cancer in men and women in the US. In 2005, an estimated 145,290 individuals were diagnosed with colorectal cancer and 56,290 will die as a result of the disease.1 Importantly, nearly 75% of the individuals diagnosed with colorectal cancer each year in the US have no known risk factor, such as family history of the disease or other predisposing condition.2 Thus, screening for CRC is strongly recommended for individuals older than age 50 years.
Colorectal cancer screening examinations include fecal occult blood test (FOBT), sigmoidoscopy, colonoscopy, and barium enema. These examinations differ in cost, acceptability, risk, effectiveness, ability to observe the colon, and patient burden.3 Mounting evidence indicates that detection and treatment of early stage colorectal cancers and adenomatous polyps can reduce colorectal cancer mortality. In particular, strong evidence from 3 case-control studies demonstrated that screening sigmoidoscopy reduces cancer mortality from tumors within reach of the sigmoidoscope by 59% to 80%.4–6
The American Gastroenterological Association (AGA) guidelines recommend that average-risk individuals aged 50 years and older undergo CRC screening.7 Similarly, the United States Preventive Services Task Force strongly urges some form of screening, either through periodic FOBT or sigmoidoscopy alone or in combination.8 The recommended screening schedules vary by type of screening examination. Screening by flexible sigmoidoscopy is recommended to be conducted every 5 years. Published data demonstrate that few people undergo the recommended screening. For example, in 2001, only 47% of age-eligible US residents reported undergoing a sigmoidoscopy or colonoscopy in the last 10 years.9 Results from previous studies that examined CRC screening are limited on the basis of self-reports or by recruitment of highly selected subjects, such as those from academic medical centers.10–13 Moreover, few studies attempted to differentiate examinations that were completed for screening versus diagnostic purposes and, thus, may have overestimated screening compliance.14, 15 In addition, few studies have examined factors that may be associated with screening compliance.
The goal of this cross-sectional study was to examine factors associated with use of screening sigmoidoscopy among men in the target age range who were at average risk for CRC and who were participants in the California Men's Health Study (CMHS), a large multiethnic cohort established within the Kaiser Permanente Northern and Southern California health plans.16
Design and Setting
The Kaiser Permanente Medical Care Program (KP) is an integrated, group practice, prepaid, health plan in 6 regions across the US. KP cares for approximately 6 million members in California, of whom 13% are older than age 50 years and, thus, targeted for colorectal cancer screening. The health plans in California offer a range of screening modalities including FOBT, flexible sigmoidoscopy, barium enema, and colonoscopy. Although flexible sigmoidoscopy is generally preferred and most commonly used for patients at average risk, the health plans support use of any screening modality based on acceptability to the patient and the clinician's recommendations.
We examined specific factors related to receipt of screening sigmoidoscopy among the CMHS cohort members. This cross-sectional study examined patient and healthcare factors associated with screening sigmoidoscopy conducted from 1998 to 2002. The cross-sectional study was nested within a prospective cohort study, the CMHS, described in detail previously.16 Briefly, the CMHS comprises male KP members from 45 to 69 years of age at the time they completed self-administered questionnaires between January 2002 to December 2003. Participants were recruited in a 2-step process. In the first step, eligible health plan members were mailed a recruitment letter and a short questionnaire. Participants who completed the short questionnaire were then mailed the long questionnaire. The long questionnaire assessed information on demographics, personal and family history of cancer, healthcare use, health conditions, medication use, and lifestyle, diet, and physical activity. At recruitment, nearly 850,000 health plan members met the eligibility criteria. Questionnaires were mailed in 3 waves, and each mailing wave included 200,000 to 350,000 members. The response varied across mailing strategies. Among men recruited for the short questionnaire, nearly 134,060 (134,060 of 848,499 or 15.8%) responded. From this group of responders (n = 134,060), a total of 84,170 (62.8%) responded to the long questionnaire. Approximately 40% of these men came from minority groups. Detailed information on recruitment and response percentages have been published elsewhere.16 The study was approved by the institutional review boards of both KP Northern California (KPNC) and KP Southern California (KPSC).
Eligible study population included CMHS participants who were between 50 to 70 years of age as of December 31, 2002, who had no personal history of CRC or colorectal polyps, and who had no family history of CRC on the basis of CMHS questionnaire data. The eligible study population also included men who were continuously enrolled from 1998 to 2002. The KPNC and KPSC guidelines recommend sigmoidoscopy as a first-line test for CRC screening because FOBT has been shown to have poor sensitivity,17 and barium enemas are unable to detect small lesions and are infrequently used because of cost. In our health plans, colonoscopies are generally recommended for diagnostic purposes such as after abnormal findings or screening higher risk patients. For these analyses, we excluded men who had previously undergone FOBTs, barium enemas, or colonoscopies during the 1997–2002 period. These procedures, along with colorectal cancer diagnosis, were ascertained from the health plans' automated databases and tumor registry.
We extracted sigmoidoscopy procedures from 1998 to 2002 from the automated health plan outpatient databases. In the KPNC region, sigmoidoscopies were identified from automated data on the basis of the CPT-4 code 45330 (flexible sigmoidoscopy). Within this group, sigmoidoscopies coded as “screening” (KPNC-specific codes) were used in the analysis. Because procedure coding in KPSC does not distinguish screening from diagnostic sigmoidoscopies, we used a validated automated data algorithm for this classification. Sigmoidoscopies were classified as diagnostic if in the year before the examination, the automated data included an encounter for specific gastrointestinal conditions (eg, Crohn disease, irritable bowel syndrome, personal history of colon polyps), or acute signs or symptoms (eg, melena, hematochezia, or rectal bleeding), or a FOBT in the 45 days before the sigmoidoscopy.18 All other sigmoidoscopies were classified into the screening group. The algorithm's sensitivity for identifying screening sigmoidoscopies was 87.9%, and the kappa between the algorithm and medical record review was 76.3%.18
Self-reported information on demographics, family history of cancer, personal history of gastrointestinal conditions, prostate specific antigen (PSA) testing, and smoking were obtained from the questionnaire. We obtained information about the department of each participant's primary healthcare provider from automated health plan databases.
We estimated the proportion of men who underwent screening sigmoidoscopy by selected demographic and healthcare factors. We calculated odds ratios and 95% confidence intervals of the association of each of these factors with screening sigmoidoscopy.
Multivariate adjusted odds ratios were estimated by using unconditional logistic regression. Factors that were significant in the bivariate analyses were included in the multivariate models. Factors were eliminated singly from the model if they did not meet the P = .025 cutoff.19 Likelihood ratio tests determined the best-fit model. All analyses were conducted by using SAS, Version 8.02 (2001; SAS Institute, Cary, NC).
A total of 64,420 cohort members met age and health plan enrollment criteria. Of these, 17,557 were excluded from the analysis because of prior colorectal cancer (n = 380) or because they had undergone colorectal screening by FOBT, colonoscopy, or barium enema (n = 17,199). We also excluded men who reported having a family history of colorectal cancer or a personal history of colon polyps. Therefore, the eligible study population included 39,559 men.
Overall, we identified 15,134 (31.6%) men who underwent screening sigmoidoscopy. The prevalence of screening sigmoidoscopy use decreased with older age and increased with higher education and household income (Table 1). Compared with whites, Asians (adjusted OR, 1.42; 95% CI, 1.30–1.56) and African Americans (adjusted OR, 1.18; 95% CI, 1.08–1.29) were more likely to have undergone sigmoidoscopy. Marital status was not strongly associated with sigmoidoscopy use, whereas residency in the US for 25 years or less was modestly associated with screening. Of note, only 24.5% of men who smoked had a screening sigmoidoscopy, and they were 25% less likely to have undergone this procedure compared with nonsmokers (adjusted OR, 0.75; 95% CI, 0.69–0.82).
Table 1. Demographic Characteristics Associated With Screening Sigmoidoscopy Use, California Men's Health Study, 1998–2002, N = 39,559
|Health plan region|
| Southern||5883 (32.1)||12404||1.00||1.00|
| Northern||6596 (31.0)||14676||0.94 (0.91–0.99)||0.85 (0.80–0.90)|
| 50–54||3266 (33.2)||6570||1.00||1.00|
| 55–59||3534 (32.8)||7216||0.99 (0.93–1.04)||0.89 (0.83–0.95)|
| 60–64||2952 (30.4)||6741||0.88 (0.83–0.94)||0.73 (0.69–0.78)|
| 65–70||2727 (29.3)||6553||0.83 (0.79–0.89)||0.67 (0.62–0.72)|
| ≥College||6417 (33.9)||12470||1.00||1.00|
| Vocational or some College||3988 (29.5)||9503||0.82 (0.78–0.86)||0.88 (0.83–0.92)|
| ≤High school||1975 (28.7)||4903||0.78 (0.74–0.83)||0.91 (0.84–0.97)|
| Missing||99 (32.6)||204||—||—|
|Marital status at time of questionnaire|
| Married/live with partner||10357 (31.7)||22317||1.00||—|
| Other||2029 (30.7)||4563||0.96 (0.90–1.01)||—|
| Missing||93 (31.7)||200||0.97 (0.76–1.24)||—|
|Current household income, $|
| ≥100,000||3743 (34.1)||7217||1.00||1.00|
| 80,000–99,999||1798 (32.7)||3698||0.93 (0.88–1.00)||0.97 (0.91–1.04)|
| 60,000–79,999||2309 (31.5)||5008||0.89 (0.83–0.95)||0.97 (0.90–1.04)|
| 40,000–59,999||2187 (30.4)||5003||0.84 (0.79–0.90)||0.94 (0.88–1.01)|
| 20,000–39,999||1538 (28.1)||3919||0.76 (0.70–0.81)||0.89 (0.81–0.96)|
| < 20,000||394 (27.1)||1058||0.72 (0.64–0.81)||0.81 (0.71–0.94)|
| Missing||510 (30.2)||1177||—||—|
| White||7656 (30.9)||17066||1.00||1.00|
| Black/African American||1079 (35.4)||1966||1.22 (1.13–1.32)||1.18 (1.08–1.29)|
| Hispanic/Latino||1512 (29.7)||3576||0.94 (0.88–1.00)||1.02 (0.94–1.10)|
| Asian||1082 (37.1)||1828||1.31 (1.22–1.43)||1.42 (1.30–1.56)|
| Other||1058 (30.5)||2404||0.98 (0.91–1.06)||1.00 (0.92–1.10)|
| Missing||92 (27.7)||240||—||—|
|Years of residence in US|
| Whole life or > 25 y||11598 (31.3)||25416||1.00||1.00|
| ≤25 y||755 (34.6)||1424||1.16 (1.06–1.27)||1.20 (1.08–1.34)|
| Missing||126 (34.4)||240||—||—|
| Nonsmoker||5534 (33.2)||11108||1.00||1.00|
| Past smoker||5624 (31.5)||12228||0.92 (0.86–0.94)||0.95 (0.90–0.99)|
| Current smoker||934 (24.5)||2875||0.65 (0.60–0.71)||0.75 (0.69–0.82)|
| Missing or unclear||387 (28.5)||869||—||—|
Men who did not undergo PSA tests were markedly less likely to undergo sigmoidoscopy compared with men who completed a PSA test (adjusted OR, 0.59; 95% CI, 0.56–0.63; Table 2). Participants who received their healthcare from providers in family practice and other primary care departments were somewhat less likely to undergo screening sigmoidoscopy than participants whose providers practiced in internal medicine departments. Sigmoidoscopy use increased with increasing numbers of outpatient visits (examined in quartiles). The associations found in Tables 1 and 2 did not change significantly after adjusting for multiple covariates.
Table 2. Healthcare Utilization Factors Associated With Screening Sigmoidoscopy Use, California Men's Health Study, 1998–2002, N = 39,559
| Yes||8027 (35.1)||14821||1.00||1.00|
| No||2517 (23.5)||8156||0.57 (0.56–0.62)||0.59 (0.56–0.63)|
| Don't know||1809 (31.9)||3850||0.87 (0.82–0.92)||0.87 (0.81–0.93)|
| Missing||126 (33.2)||253|| || |
|Primary care provider department|
| Internal medicine||7461 (33.2)||14959||1.00||1.00|
| Family practice, primarycare & other departments||4722 (30.5)||10733||0.88 (0.84–0.96)||0.82 (0.77–0.87)|
| Missing||296 (17.5)||1388||—||—|
|No. of outpatient visits1998–2002, quartiles|
| ≥38||3323 (35.6)||6011||1.00||1.00|
| 23–37||3375 (35.3)||6178||0.99 (0.93–1.04)||0.97 (0.91–1.04)|
| 13–22||3456 (33.1)||6967||0.89 (0.85–0.95)||0.88 (0.82–0.94)|
| 0–12||2325 (22.6)||7924||0.54 (0.50–0.57)||0.58 (0.54–0.62)|
We determined that demographics, socioeconomic status, specific behavioral factors, and even healthcare utilization patterns are important predictors of sigmoidoscopy screening use among average-risk men enrolled in a managed care setting. We previously reported the close similarity of the demographic distributions of CMHS participants and male participants in the California Health Interview Survey (CHIS) with respect to race and/or ethnicity, body mass index, education attainment, and income, marital status, and birthplace.16 The CHIS is a population-based multilingual telephone survey of 55,000 California residents conducted in 2001.20 Therefore, the subgroups of men identified in the present study may be important groups to target for enhanced colorectal cancer screening efforts in California.
The prevalence of screening sigmoidoscopy use decreased with older age and increased with higher education and household income. The association of age with screening could be because the analysis focused on a 5-year observation period, and patients who underwent a sigmoidoscopy could be screening compliant if they had undergone a sigmoidoscopy before this period. However, the National Health Interview Survey also noted that CRC screening generally decreased with age.21
In bivariate analyses, Asians had the highest screening prevalence (37.1%) followed by African Americans (35.4%). Overall, we found that men in the lowest socioeconomic status (SES) income category were less likely to undergo sigmoidoscopy. However, although both education attainment and income level are lower among African-American participants than white participants, African-American men were 18% more likely to undergo screening sigmoidoscopy (multivariate adjusted OR, 1.18; 95% CI, 1.08–1.29). It is possible that clinicians are more likely to recommend screening to African-American men given their higher risk of CRC. Men who lived in the US for < 25 years were 20% more likely to undergo screening (multivariate adjusted OR, 1.20; 95% CI, 1.08–1.34). This association may be driven by the finding that Asian men, who are more likely to be immigrants, had the highest screening compliance in the cohort. Although studies based on Medicare and privately insured individuals have found lower screening rates among minorities compared with white individuals, a recent study from the Veteran's Administration (VA) determined that African-American patients were 1.3 times more likely to undergo colorectal cancer screening.22 The greater use of screening by African-American and Asian patients in our managed care plans is impressive and also may be because of its similarity to VA system in terms of its general access to care. It is possible that men with higher utilization of preventive health screening or greater concern about colorectal cancer were more likely to participate in the CMHS.
Results also suggest that targeted efforts may be needed for groups with less healthy behaviors and prevention practices. Smokers who are at higher risk for many cancers may also be at higher risk for CRC-related morbidity and mortality as a result of their lower participation in CRC screening.23 Similarly, as may be expected, men who did not report PSA testing were also less likely to undergo sigmoidoscopy.
Our examination of healthcare delivery practices demonstrates missed opportunities for sigmoidoscopy screening. Whereas the likelihood of sigmoidoscopy screening increased with the number of outpatient visits, in comparison to men seen in internal medicine, men whose providers were in family practice or other primary care departments were less likely to undergo the procedure. These finding highlight the need to enhance provider education on national and health plan guidelines for screening all patients in the target age range and to test ways to promote physician adherence to those recommendations.
Previous studies have overestimated screening prevalence because their rates included diagnostic tests2, 12, 15, 24–26 and self-reports of utilization.9–14, 25–27 Strengths of this study included extraction of health plan utilization data from automated sources and use of a validated algorithm and specific CPT-4–based codes to differentiate screening from diagnostic CRC tests. Given these differences, our results are generally comparable to national reports, eg, 37% of individuals aged 50 years and older reported in the 1998 National Health Interview Survey that they had ever undergone sigmoidoscopy, and in California, the CHIS reported 54% of adults underwent some form of CRC screening in 2001.26
Despite the presence of national and health plan clinical guidelines for CRC screening and the lack of financial barriers for health plan members, less than a third of men at average risk for CRC had a screening sigmoidoscopy examination in the 5-year window of observation. The study probably underestimated screening compliance as a result of excluding FOBT, barium enema, and colonoscopy examinations during this timeframe. Nevertheless, when these tests are counted in addition to the screening sigmoidoscopies, only half of the men in the targeted age range received any of the recommended CRC screening examinations. The algorithm that we used to identify screening sigmoidoscopies in KPSC might have misclassified several screening sigmoidoscopies as diagnostic. However, the use of screening sigmoidoscopy was similar in both of the health plans (32.1% in the south and 31.0% in the north). In addition, use of automated data precluded us from examining other factors that influence compliance, such as provider recommendations and referral patterns.
In summary, the present study identified factors positively and negatively associated with screening utilization in a large, diverse population who receive health services through managed care organizations. Enhanced screening efforts should pay particular attention to men who smoke and who belong to lower socioeconomic groups. Although out-of-pocket expense is an important known barrier to CRC screening, we also determined that overall use of screening sigmoidoscopy was low (31.6%) in our insured population. The low overall screening proportion, although similar to national findings, suggests that sigmoidoscopy screening is not delivered optimally in these health plans.
Lessons learned from successful efforts to improve other preventive screening practices need to be applied to improving screening sigmoidoscopy utilization. Previous studies demonstrate that patient-reported barriers to use of screening sigmoidoscopy include lack of symptoms, worry about pain or injury, not wanting to know about health problems, being too busy, perceived susceptibility, and lack of physician recommendation.28 When providers do recommend sigmoidoscopy, patients are more likely to get screened.29 To date, the few intervention studies to promote sigmoidoscopy in primary care have met with limited success, possibly because patient perceptions of colorectal cancer screening procedures are generally negative, and confusion may exist about benefits of other screening strategies.30, 31 In their synthesis of lessons learned for promoting cancer screening, Zapka and colleagues recommend a diverse set of intervention strategies that target public policy, organizational systems, practice settings, clinicians, and patients.31 The success of multidimensional approaches has been demonstrated for breast and cervical cancer screening.31 Health plans have developed sophisticated systems to enhance other preventive screening practices, such as mammography, through patient education and provider reminder systems.32 Improved rates of screening sigmoidoscopy will require similarly comprehensive efforts.
We thank Amy Liu and Virginia Cantrell for their contributions to the study. We are also grateful to Theodore R. Levin, MD, of the Division of Research, Kaiser Permanente Northern California, for providing valuable comments on the manuscript.