Colon cancer screening, lifestyle, and risk of colon cancer

Colon cancer screening, lifestyle, and risk of colon cancer

Martha L. Slattery1,*, Sandra L. Edwards1, Khe Ni Ma1 & Gary D. Friedman21University of Utah, School of Medicine, 391 Chipeta Way Suite G, Salt Lake City, Utah USA; 2Kaiser PermanenteMedical Care Program, Division of Research, Oakland, California, USA (*Author for correspondence)

Received 11 October 1999; accepted in revised form 7 February 2000

Key words: colon cancer, colonoscopy, diet, FOB test, family history of cancer, sigmoidoscopy.

Abstract

Objectives: Sigmoidoscopy screening and fecal occult blood (FOB) tests have been demonstrated as e�ective waysto reduce mortality from colorectal cancer. However, most studies of colorectal cancer screening and cancermortality have not taken into consideration lifestyle factors that could account for the observed associations. Thepurpose of this study was to determine the association between screening and incidence of colon cancer, taking intoconsideration important lifestyle factors.Methods: We estimated the association between screening and colon cancer after taking into consideration healthand lifestyle factors using data obtained as part of population-based case±control study of incident colon cancers.Results: Sigmoidoscopy screening, especially as part of a checkup, was protective against incident colon cancer inboth men (OR 0.56, 95% CI 0.44±0.77) and women (OR 0.53, 95% CI 0.33±0.77) after adjusting for other riskfactors for colon cancer. For men, associations were stronger for distal tumors (OR 0.48, 95% CI 0.31±0.71) thanfor proximal tumors (OR 0.67, 95% CI 0.45±1.11). We did not observe signi®cant associations between FOB testand colon cancer. Di�erences in characteristics between those who were screened and not screened were alsoobserved. Men were more likely to report having a sigmoidoscopy as part of a checkup than were women, as werepeople with higher levels of education. People who reported having a sigmoidoscopy as part of a checkup alsoreported eating diets lower in fat and higher in ®ber, folate, and vegetables. Men were more likely to report higherlevels of physical activity, and women were more likely to report taking hormone replacement therapy (HRT) if theyalso reported a sigmoidoscopy. Both men and women who reported a sigmoidoscopy for screening purposes weremore likely to have a family history of colorectal cancer.Conclusions: These data provide additional support for the bene®ts of having a screening sigmoidoscopy. Theassociations between screening sigmoidoscopy and colon cancer do not appear to be the result of lifestyle factors.

Introduction

Colorectal cancer is the third leading cause of cancerincidence and mortality in US men and women [1].Screening can lead to early detection of colorectal cancerand, by removal of polyps, can often prevent cancerdevelopment. Two tests, fecal occult blood (FOB) andsigmoidoscopy, have been recommended for colorectalcancer screening. Results on the e�cacy of FOB testsare mixed [2±4] from observational mortality studies,although three clinical trials have shown signi®cantreductions in colorectal cancer mortality as a result ofFOB tests [5±7]. Screening sigmoidoscopies, while notexamined in clinical trails, have been associated consis-

tently with lower mortality and incidence from colorec-tal cancer [8±12]. Unanswered questions remain in termsof colorectal cancer screening. First, is screening asso-ciated with reduced incidence as well as reducedmortality from colorectal cancer? Second, are theassociations between screening and colorectal cancerthe result of uncontrolled confounding of other healthbehaviors that are associated with both screening andcolorectal cancer? Third, what are the characteristics ofthe population not being screened?In this study we use data collected as part of a case±

control study of colon cancer to estimate the associationbetween sigmoidoscopy and FOB test and incidence ofcolon cancer. We evaluate the health and lifestyle

Cancer Causes and Control 11: 555±563, 2000. 555Ó 2000 Kluwer Academic Publishers. Printed in the Netherlands.

characteristics between screened and unscreened popu-lations to better identify factors that could confoundthese associations. We also evaluate characteristics ofthose who do not report screening.

Methods

Study population

Data for this study come from a large multi-center studyof colon cancer. Included in these analyses are partic-ipants identi®ed from the Kaiser Permanente MedicalCare Program (KPMPC) of Northern California and aneight-county area in Utah. Study participants from theTwin Cities Metropolitan area in Minnesota are notincluded because of lower response rates from that areathat may in¯uence results focusing on screening withinthe context of a case±control study [13]. All cases werebetween the ages of 30 and 79 and had a ®rst primarycolon cancer (ICD-O, 2nd edition codes 18.0, 18.2 to18.9) veri®ed through a SEER registry for KPMCP andUtah. Cases of the rectosigmoid junction and rectumwere not eligible for the study since the focus of thestudy was on the etiology of colon cancer, and there aresuggestions that di�erences may exist for colon andrectal cancer cases in terms of etiology. Cases withidenti®ed familial adenomatous polyposis, ulcerativecolitis, or Crohn's disease also were excluded from thestudy. Control selection methods have been reportedelsewhere [14, 15]; at KPMCP controls were randomlyselected from membership lists and in Utah controlswere identi®ed using Health Care Financing Adminis-trations lists (age 65 and older), driver's license list, orrandom-digit-dialing. Controls were matched to cases(using a 1:1 matching ratio) by sex and 5-year agegroups. Response rates (the proportion of all eligiblepeople identi®ed who participated in the study), coop-eration rates (the proportion of all eligible peoplecontacted who participated in the study), and contactrates (the proportion of all eligible people who we wereable to contact, i.e. physician refusal and those whowere dead are not included in the denominator) werecalculated as described [15]; for the KPMCP and Utahcenters these rates were 71.8% (response), 80.8%(cooperation), and 98.6% (contact) for cases and 68.0,71.6, and 95.6% respectively for controls. The mediantime from diagnosis to identi®cation was 17 days forKPMCP and 24 days for Utah. Of the cases who did notparticipate, 35.8% were too ill to complete the interviewor were deceased before the interview could be com-pleted. Another 11.2% were not contacted because ofphysician refusal, 48.6% refused to participate, and

4.4% either moved, could not be located, or did notparticipate for other reasons.

Data ascertainment

Study participants were interviewed by trained andcerti®ed interviewers using a computerized question-naire [16, 17]. Interviewers were trained by study sta�and demonstrated a high level of performance prior tobeing able to conduct interviews on study participants[16, 17]. The interview lasted approximately 2 hours.The referent period for study questions was the calendaryear 2 years before diagnosis for cases or selection forcontrols. Screening history during the 10 years prior toand including the referent year was obtained to getinformation about screening during a time prior todisease that would be relevant to the disease process[10]. Participants were asked if they had a sigmoidos-copy test de®ned as: ``This test involves a doctorexamining your rectum with a long tube with a lighton it. It is a deeper examination than an anoscope examwhich looks at conditions such as hemorrhoids and®ssures in the anus or opening of the rectum.'' Partic-ipants were also asked if they had a FOB test, which wasdescribed as a ``test to see if there was blood in yourbowel movement. This is sometimes called a hemocculttest. It is usually done by having you put a small bit ofbowel movement on a special card.'' Participants whoreported ``yes'' to either of these questions were thenasked a series of questions to determine if the tests weredone for problems (i.e., rectal bleeding, constipation,diarrhea, pain in the rectum or belly, or other conditionsor symptoms), or ``as part of a checkup and not becauseof symptoms''. The number of times the tests were doneduring the 10-year exposure period for problems and aspart of a checkup was determined.Dietary data were obtained using an adaptation of the

validated CARDIA diet history questionnaire [17] andwere converted to nutrient values using the NutritionCoordinating Center (NCC) nutrient database. Usualalcohol consumption was estimated from the diethistory questionnaire; consumption on weekdays (Mon-day through Thursday) and weekend days (Fridaythrough Sunday) was reported separately. Physicalactivity data were obtained using an adaptation of theCARDIA physical activity history [18]; similar ques-tions were asked for activity patterns 10 and 20 yearsago. Other data included: measured height and self-reported weight for the referent period and for 5 yearsprior to diagnosis; cigarette smoking history (everhaving smoked on a regular basis, year started andstopped, and usual amount smoked); reproductivehistory, hormone replacement therapy (HRT); medical

556 M.L. Slattery et al.

history; drug use history which included questions aboutaspirin and other non-steroidal anti-in¯ammatory drugs(NSAIDs); family history of cancer among ®rst-degreerelatives, and history of having colonic polyps.

Statistical methods

Di�erences in the proportion of the population screenedby various population characteristics were determinedusing v2 test. This information was assessed for thoseonly having screening as part of a checkup as well as foreveryone who reported having received the test eitherfor screening or due to a problem. We further evaluatedthe di�erences by screening in the age-adjusted meanlevels of health and lifestyle characteristics among casesand controls using analysis of covariance. These ana-lyses were done for men and women separately. Finally,using unconditional logistic regression analyses, wedetermined the impact of adjustment of confoundingfactors on estimated associations between screening andcolon cancer. Age- and site-speci®c analyses were done.Proximal tumors were de®ned as those tumors in thececum through the transverse colon; distal tumors werede®ned as those tumors in the splenic ¯exure, descend-ing, or sigmoid colon.

Results

Controls who received health care from an HMO weremore likely to have screening for a checkup thancontrols who were randomly selected from the popula-tion (Table 1). Male cases and controls were more likelyto report sigmoidoscopy screening for a checkup thantheir female counterparts. Older people were more likelyto report having had a sigmoidoscopy for screening for acheckup than younger people and those with moreeducation. Participants who were Hispanic were morelikely to report not having been screened as part of acheckup in the past 10 years, while black controls weremore likely to report having been screened as part of acheckup. There were no statistically signi®cant di�er-ences in screening for checkup purposes by income ormarital status.The most common reason for sigmoidoscopy screen-

ing for men was for a checkup (Table 2), althoughwomen who were cases were equally as likely to report asigmoidoscopy for problems as for a checkup. The mainreason for having a FOB test was for screeningpurposes. There was a signi®cant association betweenhaving a FOB for screening purposes and having asigmoidoscopy for screening purposes (p = <0.01). Ofthose who received the test either for screening or due to

a problem, twice as many male cases and almost threetimes as many female cases reported having had polypsas did controls who had the same tests.Having a sigmoidoscopy during the past 10 years was

associated with a halving of risk of developing coloncancer (Table 3). This association was observed for bothmen and women. Further adjustment for other dietaryfactors such as folate, red meat intake, or other lifestylefactors did not alter these associations. Among men, theassociations was strongest for the tumors in the distalsegment of the colon. Having a FOB screening test wasalso associated with reduced risk among men, but themagnitude was less (OR 0.8) and statistical signi®cancewas borderline (95% CI 0.6±1.1).Assessment of diet and lifestyle factors that may be

associated with screening did reveal some signi®cantdi�erences between those who reported screening for acheckup and those who reported never having the testfor either a problem or as part of a checkup. Moresigni®cant di�erences in health and lifestyle factors wereobserved for sigmoidoscopy than for FOB and areshown in Table 4. People who reported a sigmoidoscopyas part of a checkup were more likely to consume dietslower in fat (women cases p = 0.01) and higher in ®ber(male controls p < 0.01), folate (male controlsp < 0.01), and vegetables (male cases p = 0.04),although the magnitude of the di�erences varied formen and women and by case/control status. Womencases who reported sigmoidoscopy screening as part of acheckup were also more likely to report taking HRT(p = 0.05) and male controls reported signi®cantlymore physical activity (p = <0.01). People who had afamily history of colorectal cancer were more likely toreport having a sigmoidoscopy as part of a checkupduring the past 10 years (statistically signi®cant only forwomen). Results only varied slightly when those whohad a sigmoidoscopy as the result of a problem wereincluded in the analysis.

Discussion

Evaluation of a cancer screening test by an observa-tional epidemiologic study is normally directed atdetermining whether its use is negatively associated withthe outcome it is designed to prevent, usually fatal ormetastatic cancer [13]. It is hoped that the test will leadto early detection, prompt treatment, and cure. In thisstudy we observed a negative association of screeningtests with the occurrence of incident colon cancerirrespective of stage or fatality. This association wasobserved for both men and women. If our results arevalid and not due to chance, information bias, or

Lifestyle, screening, and colon cancer 557

uncontrolled confounding, the means by which thesefavorable ®ndings could have occurred is by thedetection and removal of premalignant polyps, prevent-ing their progression to cancer. In this study, cases weretwo to three times more likely to have had polyps thancontrols who reported having a sigmoidoscopy.We believe that the present analysis of our large case±

control study adds to the evidence that sigmoidoscopy isan e�cacious preventive modality, but our approachdi�ered from conventional studies of screening tests forlarge bowel cancer in which the cases were restricted topersons with fatal disease [8, 10]. Our study is like moststudies of pap smears, in which the cases were womenwith invasive cervical cancer diagnosed at any stage [19].

Data from this study strengthen previous reports of theinverse association between sigmoidoscopy screeningand development of colon cancer, since adjustment forother health and lifestyle factors did not alter the inverseassociation. We also observed, in this population, thatthere were di�erences in the proportion screened ac-cording to sex, level of education, race, and study center.Utilization of case±control studies to evaluate screen-

ing has several potential limitations [13, 19±22]. Weissand Lazovich [13] presented three validity criteria forthe use of a conventional interview-based case±controlstudy such as ours as the basis for a more standardevaluation of a cancer screening test, in which attentionis restricted to the advanced or fatal cases within the

Table 1. Demographic characteristics of the population by screening statusa

Sigmoidoscopy screening

Cases Controls

Yes

n (%)bNo

n (%)

p-Value Yes

n (%)

No

n (%)

p-Value

Location

Kaiser (HMO) 119 (15.8) 635 (84.2) 0.85 204 (26.6) 564 (73.4) 0.04

Utah (population) 45 (15.3) 249 (84.7) 94 (21.3) 347 (78.7)

Sex

Men 105 (17.8) 486 (82.2) 0.03 193 (28.7) 480 (71.3) <0.01

Women 59 (12.9) 398 (87.1) 105 (19.6) 431 (80.4)

Age at diagnosis (years)

<50 2 (2.5) 78 (97.5) <0.01 6 (4.3) 134 (95.7) <0.01

50±67 66 (14.5) 388 (85.5) 110 (23.0) 369 (77.0)

>67 96 (18.7) 418 (81.3) 182 (30.9) 408 (69.2)

Education level

<High school 23 (13.3) 150 (86.7) 0.04 33 (23.2) 109 (76.8) 0.04

High school 35 (12.6) 242 (87.4) 86 (25.4) 252 (74.6)

Some advanced 58 (15.1) 326 (84.9) 85 (20.4) 332 (79.5)

College graduate 21 (21.9) 75 (78.1) 41 (27.0) 111 (73.0)

Post-college 27 (22.9) 91 (77.1) 52 (32.7) 107 (67.3)

Income

<$20,000 30 (12.0) 220 (88.0) 0.37 60 (21.6) 218 (78.4) 0.36

$20,000±$35,000 48 (16.6) 241 (84.0) 84 (27.7) 219 (72.3)

$35,001±$50,000 37 (16.4) 188 (83.6) 71 (27.2) 190 (72.8)

$50,001±$60,000 10 (13.0) 67 (87.0) 23 (22.8) 78 (77.2)

>$60,000 24 (18.9) 103 (81.1) 45 (22.8) 152 (77.2)

Marital status

Married 123 (16.2) 637 (83.8) 0.53 230 (25.4) 676 (74.6) 0.49

Widowed, divorced,

or separated

36 (13.7) 227 (86.3) 63 (22.9) 212 (77.1)

Never married 5 (20.0) 20 (80.0) 5 (17.9) 23 (82.1)

Race

White 147 (16.3) 757 (83.7) 0.40 259 (24.1) 814 (75.9) <0.01

Black 10 (13.0) 67 (87.0) 25 (41.0) 36 (59.0)

Hispanic 7 (10.8) 58 (89.2) 13 (17.6) 61 (82.4)

a Screening for checkup only; excludes people who had screening for a problem.b Percent of category of cases and of controls, i.e. percent of male cases who had screening.


study. These criteria must also be considered withrespect to our study. The ®rst is a ``very high responserate to the interview or questionnaire''. Failure toinclude the very ill or dying cases could increase theproportion of screen-detected cancers, leading to anunderestimate of the e�cacy of screening. In the contextof cases who participated in this study, one of the majorreasons for non-participation was death and illness [23].Given the more advanced stage of these cases at the timeof diagnosis, it is likely that they did not have screening.Exclusion of these cases would result in an overestimateof the percentage of cases screened in the studypopulation compared to the target population with anunderestimation of the e�cacy of screening. However,controls who did not participate might also be less likelyto have undergone screening than those who didparticipate, if people who are more health-consciousare more likely to participate in studies such as this.Overall, these e�ects would most likely result in atten-uated associations between colon cancer and screeningsigmoidoscopy.The second criterion put forth by Weiss and Lazovich

[13] for the evaluation of screening requires the accuratereporting of the fact and the timing of, and reason for,each screening test.

Depending on the nature and extent of these errors,the estimate of screening e�cacy could be biased eitherupward or downward. In this study, screening data wereself-reported, as is the case in most studies of screening[4, 8, 9]. However, past studies that have validatedrecalled screening behaviors against medical recordshave shown that events such as sigmoidoscopy screeningare recalled with over 80% validity [24]. A recentvalidation study of participants at the Kaiser Perma-nente Medical Care Program (KPMCP) provides addi-tional information on self-reported screening practicesfor 95 participants from the study [25]. The percentagreement between self-reported and medical recordaudit was 71% of FOB and 81% for sigmoidoscopy forscreening purposes. These ®gures increased when re-ported colonoscopies were included as screening eventsthat occurred within 2 years of the 10-year target timeinterval. Others have also reported that, although peopleremember events such as screening sigmoidoscopy,details as to time of event and number of times havingbeen screened are reported with less reliability [26, 27].Other studies have shown that major events such assigmoidoscopy screening are easier to remember thanevents that are relatively minor (i.e, eating a carrot) [28].The study by Habel and colleagues [25] also suggests

Table 2. Screening characteristics of study population (®gures in parentheses are percentages)

Men Women

Cases (n = 756) Controls (n = 845) Cases (n = 590) Controls (n = 699)

Screening test

Sigmoidoscopy

Never 486 (73.4)b 480 (62.9) 398 (79.8) 431 (70.1)

Evera 176 (26.6) 283 (37.1) 101 (20.2) 184 (29.9)

For problems 79 (12.0) 109 (14.3) 51 (10.2) 88 (14.4)

For checkup 105 (16.0) 193 (25.4) 59 (11.9) 105 (17.2)


30±49 4 (2.3) 9 (3.2) 10 (9.9) 6 (3.3)

50±67 78 (44.3) 118 (41.7) 42 (41.6) 81 (44.0)

>67 94 (53.4) 156 (55.1) 49 (48.5) 97 (52.7)

FOB test

Never 289 (43.4) 283 (36.6) 209 (41.6) 240 (38.7)

Ever 377 (56.6) 491 (63.4) 293 (58.4) 380 (61.3)

For problems 76 (11.6) 96 (12.6) 62 (12.4) 65 (10.6)

For check-up 316 (48.0) 417 (54.4) 240 (48.5) 329 (53.4)


30±49 16 (4.2) 27 (5.5) 18 (6.1) 18 (4.7)

50±67 174 (46.2) 205 (41.8) 140 (47.8) 172 (45.3)

>67 187 (49.6) 259 (52.7) 135 (46.1) 190 (50.0)

Ever have polyps

Yesc 59 (33.5) 50 (17.9) 38 (38.0) 26 (14.2)

No 117 (66.5) 230 (82.1) 62 (62.0) 157 (85.8)

a Ever de®ned as having had during the 10-year period being questioned. Individuals could report test for both problems and checkup.b Percent of cases or controls.c Polyp status is based on percent of study participants who ever reported having a sigmoidoscopy test.


that the accuracy of reported screening events did notdi�er markedly by age, gender, or case/control status.This implies that estimates of the association presentedhere are biased towards the null and therefore representconservative estimates of the protective e�ect.Closely tied into the second criterion put forth by

Weiss and Lazovich [13] is the ability of study partic-ipants to distinguish between a colonoscopy and sig-moidoscopy. It may be, given the similar associationsfor proximal and distal tumors in women, that partic-ipants reported colonoscopies rather than sigmoidos-copies. In the study by Habel et al. [25], approximately12.5% of those who reported a sigmoidoscopy thatcould not be veri®ed in the medical records actually hada colonoscopy. Since approximately half of women whoreported having had sigmoidoscopies had them as aresult of problems, it is possible that the test performedwas actually a colonoscopy. Furthermore, since therecommended screening at Kaiser Permanente for thosewith a family history of colorectal cancer, for previous

premalignant polyps, or for certain symptoms such asin¯ammatory bowel syndrome, is a colonoscopy ratherthan a sigmoidoscopy it is possible that some of thosewho reported a sigmoidoscopy actually had a morethorough screening in the form of a colonoscopy.However, if colonoscopy was the recommended modeof screening rather than sigmoidoscopy, inclusion ofthose who had colonoscopies as part of the screenedpopulation is justi®ed since they would not have had theopportunity to have a sigmoidoscopy. This could,however, slightly in¯ate the association for sigmoidos-copy compared with when colonoscopies had not beenincluded by some individuals.In this study we evaluated those who had a sigmoi-

doscopy as part of a checkup as well as those who had asigmoidoscopy for a problem. Results were slightlystronger if analyses only included those with a sigmoi-doscopy as part of a checkup compared with when thosewho had a sigmoidoscopy because of a problem alsowere included. Some studies have limited their sample to

Table 3. Associations between reported sigmoidoscopy and FOB tests and risk of incident colon cancer

Men Women

Age-adjusted

OR (95% CI)

Full modela

OR (95% CI)

Age-adjusted

OR (95% CI)

Full model

OR (95% CI)

Ever any sigmoidoscopy

All subjects 0.6 (0.5±0.8) 0.6 (0.5±0.8) 0.6 (0.4±0.8) 0.6 (0.4±0.8)

<67 years 0.6 (0.5±0.9) 0.7 (0.5±1.1) 0.6 (0.4±0.9) 0.6 (0.4±0.9)

³67 years 0.6 (0.4±0.8) 0.6 (0.4±0.8) 0.6 (0.4±0.8) 0.6 (0.4±0.8)

Distal tumors 0.5 (0.4±0.7) 0.5 (0.4±0.7) 0.6 (0.4±0.8) 0.6 (0.4±0.8)

Proximal tumors 0.8 (0.6±1.04) 0.8 (0.6±1.1) 0.6 (0.4±0.8) 0.6 (0.4±0.8)

Ever sigmoidoscopy for checkupb

All subjects 0.5 (0.4±0.7) 0.6 (0.4±0.8) 0.5 (0.4±0.8) 0.5 (0.3±0.8)

<67 years 0.5 (0.4±0.8) 0.6 (0.3±0.8) 0.6 (0.3±1.1) 0.6 (0.4±1.1)

³67 years 0.6 (0.4±0.8) 0.6 (0.3±0.8) 0.5 (0.3±0.6) 0.5 (0.3±0.8)

Distal tumors 0.5 (0.3±0.7) 0.5 (0.3±0.7) 0.5 (0.3±0.6) 0.5 (0.3±0.9)

Proximal tumors 0.7 (0.4±1.0) 0.7 (0.5±1.1) 0.6 (0.4±0.9) 0.5 (0.3±0.9)

Ever any FOB test

All subjects 0.8 (0.3±1.03) 0.8 (0.7±1.04) 1.0 (0.8±1.4) 1.1 (0.8±1.4)

<67 years 0.8 (0.6±1.1) 0.8 (0.6±1.1) 1.0 (0.7±1.4) 1.1 (0.7±1.7)

³67 years 0.7 (0.5±1.03) 0.8 (0.6±1.1) 1.0 (0.7±1.4) 1.1 (0.7±1.7)

Distal tumors 0.8 (0.6±1.1) 0.9 (0.7±1.1) 1.1 (0.8±1.7) 1.3 (0.8±1.7)

Proximal tumors 0.8 (0.6±1.1) 0.8 (0.6±1.1) 1.0 (0.7±1.4) 1.1 (0.8±1.4)

Ever FOB test for checkupb

All subjects 0.8 (0.6±1.03) 0.8 (0.6±1.01) 1.0 (0.7±1.3) 1.0(0.8±1.4)

<67 years 0.8 (0.6±1.3) 0.8 (0.5±1.1) 0.8 (0.5±1.3) 0.8 (0.5±1.3)

³67 years 0.7 (0.5±1.0) 0.7 (0.5±1.1) 1.1 (0.8±1.7) 1.1 (0.8±1.7)

Distal tumors 0.8 (0.6±1.1) 0.8 (0.6±1.1) 1.0 (0.7±1.4) 1.0 (0.7±1.7)

Proximal tumors 0.8 (0.6±1.1) 0.8 (0.6±1.1) 1.0 (0.7±1.4) 1.0 (0.7±1.4)

a All associations are comparing those without screening to those who reported screening Full model adjusted for age, BMI, total energy

intake, physical activity, use of aspirin/NSAIDs, family history of colorectal cancer, dietary ®ber, calcium and cholesterol. Further adjustment for

HRT use among women only slightly altered ®ndings, i.e. OR for all subjects 0.50 (95% CI 0.33±0.77) versus 0.53 for ever having a screening

sigmoidoscopy as part of a checkup.b Analyses evaluating checkups exclude those who had screening because of a problem.


those who had a sigmoidoscopy as part of a checkup[10]. However, it can be argued that a sigmoidoscopyperformed as the result of having a problem wouldgreatly decrease the likelihood of having a sigmoidos-copy for a checkup. The outcome of the sigmoidoscopy,removal of polyps that could potentially develop intotumors, would be the same for both scenarios.

The third criterion discussed by Weiss and Lazovich[13] requires long follow-up of the incident cases,su�cient to give all subsequent metastases or fatalityto be manifest. This does not apply to our study, whichfocuses on all incident cancers. Somewhat linked to thiscriterion is the need to capture screening information forthe relevant time when screening would be most e�ective

Table 4. Age-adjusted mean levela of lifestyle factors among those who had a sigmoidoscopy for screening purposes

Cases Controls

Sigmoidoscopy

(n = 164)

No

sigmoidoscopy

(n = 884)

P-Value Sigmoidoscopy

(n = 298)

No

sigmoidoscopy

(n = 911)

p-Value

BMIb

Men 27.5 28.2 0.20 27.0 27.2 0.69

Women 34.3 34.3 0.91 34.2 33.5 0.46

Physical activity indexc

Men 7.3 6.7 0.10 8.2 7.2 <0.01

Women 5.8 5.9 0.81 6.3 6.4 0.74

Daily dietary intake Fat (g/1000 kcal)

Fat (g/1000 kcal)

Men 36.6 37.2 0.52 35.1 36.2 0.09

Women 33.7 36.4 0.01 34.0 35.0 0.26

Calcium (mg/day)

Men 1244 1169 0.32 1287 1177 0.06

Women 977 950 0.79 970 987 0.84

Fiber (g)

Men 28.6 26.4 0.17 29.4 26.5 <0.01

Women 24.8 22.1 0.19 23.6 23.7 0.95

Folate (lg)Men 460 420 0.12 482 408 <0.01

Women 372 349 0.34 350 365 0.45

Vegetablesd

Men 4.2 3.5 0.04 3.9 3.9 0.81

Women 3.8 3.8 0.98 4.2 4.1 0.53

Red meatd

Men 0.8 0.9 0.11 0.8 0.8 0.73

Women 0.6 0.6 0.36 0.5 0.6 0.19

Alcohol (g)

Men 22.2 19.9 0.57 19.4 15.6 0.24

Women 10.1 8.8 0.64 7.2 8.1 0.75

Smokers (% ever)

Men 73.3 71.2 0.66 57.0 60.4 0.41

Women 35.6 46.7 0.11 41.0 39.0 0.71

Aspirin use (% yes)

Men 25.7 30.3 0.36 36.3 34.8 0.72

Women 23.7 21.9 0.75 30.5 29.9 0.91

NSAID use (% yes)

Men 32.4 39.5 0.17 49.2 44.8 0.30

Women 39.0 38.4 0.94 49.5 46.4 0.57

HRT (% yes)

Women 56.1 42.3 0.05 55.9 48.5 0.42

Family history (% colorectal cancer)

Men 20.2 14.6 0.17 11.4 7.5 0.10

Women 22.0 12.8 0.06 26.7 6.3 <0.01

a Age-adjusted means calculated from analysis of covariance; excludes individuals who had a sigmoidoscopy as a result of a problem.b BMI for men is weight/height2 and for women is weight/height1.5.c Based on activity score from 3 to 12.d Standard serving of vegetables is � cup; standard serving of red meat is 3 ounces.


[29]. In this study we asked participants to reportscreening performed during the 10 years prior to andincluding the referent year. We believe that this referentperiod is the most relevant time for the detection andremoval of colonic polyps that could progress to cancer.Given our results, and potential study limitations,

several di�erences were observed in this population ofsigmoidoscopy screened vs. unscreened individuals. Ingeneral, people who reported a sigmoidoscopy forscreening were more likely to consume a diet that ishigher in folate, ®ber, and calcium and lower in red meatand fat, although there were variations between men andwomen as to the magnitude of these di�erences. Eval-uation of health and lifestyle characteristics in men beingfollowed as part of the Health Professionals' Follow-upStudy showed similar associations to those reported here[9]. Having a family history of colorectal cancer, a riskfactor for colorectal cancer [30], also increased theprobability of reporting a screening sigmoidoscopy. It ispossible that those with a family history of colorectalcancer more accurately report their screening events thanthose without a similar family history, since they may bemore familiar with the test. Familiarity with screeningtests has been shown to improve accuracy in reportingscreening [28]. Although population characteristics dif-fered between those who reported a screening sigmoi-doscopy and those who did not, reporting asigmoidoscopy screening was inversely associated withcolon cancer after taking into consideration these di�er-ences in health, lifestyle, and family history.This study points to di�erences in screening practices

within the population. In this population those mostlikely to be screened were HMO members, men, andpeople who had more education. Additionally, Hispanicpeople were less likely to report a screening sigmoidos-copy than either white or black study participants. Ahigh level of screening reported among black studyparticipants could be the result of availability ofscreening through KPMCP. Women who reported asigmoidoscopy were more likely than men to report it asthe result of a problem rather than as part of a checkup.It is unknown if patterns of care are di�erent for womenthan men. Although it is generally believed that womenare more apt to seek medical care than men, it is possiblethat health-care providers from whom women receivecare, are less likely to recommend screening sigmoidos-copy than they are for men. These di�erences inscreening sigmoidoscopy practices point to groups inthe population who should be targeted for screeningpromotion programs.In summary, these data support other studies as to the

e�cacy of sigmoidoscopy screening in the prevention ofcolon cancer. Despite health and lifestyle di�erences

among those who report screening and those who donot, the protective e�ect of screening remains. However,given the di�erences observed in reported screeningpractices for men and women, by education level, andby race, cancer control activities should attempt to stressthe value of screening to all segments of the populationas a means to reduce the incidence of colorectal cancer.

Acknowledgements

This study was funded by grants CA48998 to DrSlattery and CA49761 to Dr Friedman. Case identi®ca-tion and veri®cation were supported by the Utah CancerRegistry contract NONC1-CN-67000 and support fromUtah Dept. of Health, the Northern California CancerRegistry, and the Sacramento Tumor Registry. Wewould like to acknowledge the contributions and sup-port of Dr Bette Caan to this study. The contents of thispaper are solely the responsibility of the authors and donot necessarily represent the o�cial view of the NationalCancer Institute.

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Colon cancer screening, lifestyle, and risk of colon cancer