Background The influence of excess body weight on the risk ofdeath from cancer has not been fully characterized.
Methods In a prospectively studied population of more than 900,000U.S. adults (404,576 men and 495,477 women) who were free ofcancer at enrollment in 1982, there were 57,145 deaths fromcancer during 16 years of follow-up. We examined the relationin men and women between the body-mass index in 1982 and therisk of death from all cancers and from cancers at individualsites, while controlling for other risk factors in multivariateproportional-hazards models. We calculated the proportion ofall deaths from cancer that was attributable to overweight andobesity in the U.S. population on the basis of risk estimatesfrom the current study and national estimates of the prevalenceof overweight and obesity in the U.S. adult population.
Conclusions Increased body weight was associated with increaseddeath rates for all cancers combined and for cancers at multiplespecific sites.
The relations between excess body weight and mortality, notonly from all causes but also from cardiovascular disease, arewell established.1,2,3,4,5,6 Although we have known for sometime that excess weight is also an important factor in deathfrom cancer,7 our knowledge of the magnitude of the relation,both for all cancers and for cancers at individual sites, andthe public health effect of excess weight in terms of totalmortality from cancer is limited.
Previous studies have consistently shown associations betweenadiposity and increased risk of cancers of the endometrium,kidney, gallbladder (in women), breast (in postmenopausal women),and colon (particularly in men).8,9,10,11,12 Adenocarcinomaof the esophagus has been linked to obesity.11,13,14 Data oncancers of the pancreas, prostate, liver, cervix, and ovaryand on hematopoietic cancers are scarce or inconsistent.7,8,9,10,11,15,16,17The lack of consistency may be attributable to the limited numberof studies (especially those with prospective cohorts), thelimited range and variable categorization of overweight andobesity among studies, bias introduced by reverse causalitywith respect to smoking-related cancers, and possibly real differencesbetween the effects of overweight and obesity on the incidenceof cancer and on the rates of death from some cancers.18,19
We conducted a prospective investigation in a large cohort ofU.S. men and women to determine the relations between body-massindex (the weight in kilograms divided by the square of theheight in meters) and the risk of death from cancer at specificsites. This cohort has been used previously to examine the associationof body-mass index and death from any cause.5
Methods
Study Population
The men and women in this study were selected from the 1,184,617participants in the Cancer Prevention Study II, a prospectivemortality study begun by the American Cancer Society in 1982.20,21The participants were identified and enrolled by more than 77,000volunteers in all 50 states, the District of Columbia, and PuertoRico. Families were enrolled if at least one household memberwas 45 years of age or older and all enrolled members were 30years of age or older. The average age of the participants atenrollment was 57 years. In 1982 they completed a confidentialmailed questionnaire that included personal identifiers andelicited information on demographic characteristics, personaland family history of cancer and other diseases, and variousbehavioral, environmental, occupational, and dietary exposures.
Over 99 percent of deaths that occurred from the month of enrollmentuntil September 1988 were ascertained by means of personal inquiriesmade by volunteers in September 1984, 1986, and 1988.22 Approximately93 percent of all deaths occurring after September 1988 wereascertained by linkage with the National Death Index.22 By December31, 1998, 24.0 percent of the participants had died, 75.8 percentwere still living, and 0.2 percent were dropped from follow-upon September 1, 1988, because of insufficient data for linkagewith the National Death Index. Death certificates or multiplecause-of-death codes were obtained for 98.8 percent of all knowndeaths.
In the base-line questionnaire, the participants were askedtheir current weight, weight one year previously, and height(without shoes). We excluded from the analysis participantswhose values for height or weight were missing, whose weightone year before the interview was unknown, or who had lost morethan 10 lb (4.5 kg) in the previous year; 65,436 men and 91,282women were excluded for these reasons. We also excluded participantswith below-normal weight according to World Health Organizationguidelines23 as indicated by a body-mass index of less than18.5 (3393 men and 15,769 women). In addition, we excluded participantswho had cancer (other than nonmelanoma skin cancer) at baseline (20,839 men and 47,120 women) and those with missing informationon race or smoking history (14,086 men and 26,639 women). Theeligible participants for the current analysis included 404,576men and 495,477 women. After 16 years of follow-up, there werea total of 32,303 deaths from cancer in men and 24,842 deathsfrom cancer in women in this population.
From the final population of 900,053 participants, we defineda subgroup of those who had never smoked (107,030 men and 276,564women). Within this subgroup, there were a total of 5314 deathsfrom cancer among men and 11,648 among women. This subgroupprovided us with an opportunity to evaluate whether the associationbetween body-mass index and mortality was subject to residualconfounding by smoking status for smoking-related cancers.
Body-Mass Index
The body-mass index, a measure of adiposity, was categorizedas follows: 18.5 to 24.9, 25.0 to 29.9, 30.0 to 34.9, 35.0 to39.9, and 40.0 or more. These categories correspond to thoseproposed by the World Health Organization23 for "normal range,""grade 1 overweight," "grade 2 overweight" (30.0 to 39.9), and"grade 3 overweight," respectively. For many analyses, especiallyfor cancers in specific sites and among participants who hadnever smoked, the upper categories of body-mass index were combined,because of the small numbers. In our analyses and discussion,we refer to the range of 25.0 to 29.9 as corresponding to "overweight"and to values of 30.0 or more as corresponding to "obesity."
In all primary analyses, the body-mass index category of 18.5to 24.9 ("normal range") was considered the reference group.We also conducted analyses in which we divided this group intotwo categories of 18.5 to 22.9 and 23.0 to 24.9 and consideredthe lower category to be the reference group.
Mortality End Points
The end points in our analyses were deaths from all cancers(codes 140.0 to 195.8 and 199.0 to 208.9 of the InternationalClassification of Diseases,Ninth Revision [ICD-9])24 and fromcancers at selected sites. Specific cancers accounting for atleast 150 deaths in men and 150 deaths in women included esophagealcancer (ICD-9 codes 150.0 to 150.9), stomach cancer (151.0 to151.9), colorectal cancer (153.0 to 154.8), liver cancer (155.0to 155.2), gallbladder cancer (156.0 to 156.9), pancreatic cancer(157.0 to 157.9), lung cancer (162.0 to 162.9), melanoma (172.0to 172.9), breast cancer in women (174.0 to 174.9), cancer ofthe corpus and uterus, not otherwise specified (179 and 182.0to 182.8), cervical cancer (180.0 to 180.9), ovarian cancer(183.0 to 183.9), prostate cancer (185), bladder cancer (188.0to 188.9), kidney cancer (189.0 to 189.9), brain cancer (191.0to 191.9), non-Hodgkin's lymphoma (202.0 to 202.9), multiplemyeloma (203.0 to 203.8), and leukemia (204.0 to 208.9). Allother specific cancers that contributed to total deaths fromcancer but that caused fewer than 150 deaths or were coded asunspecified (199.0 to 199.1) were analyzed as a separate categoryof "other" cancers. Approximately 11 percent of cancers in bothmen and women fell into the "other" category. Of these, 45 percenthad a specific (coded) site and caused fewer than 150 deathsand 55 percent had a site that was coded as unspecified. Dataregarding cancer subsites or histologic findings were not available.
Information on Covariates
Potential confounders included in data analyses were age (insingle years), race (white, black, or other), smoking status(never smoked, formerly smoked, or currently smokes, with threecategories of cigarettes smoked per day: 0 to 19, 20, and morethan 20), education (less than high school, high-school graduate,some college, or college graduate), physical activity (none,slight, moderate, or heavy), alcohol use (none, less than onedrink per day, one drink per day, or two or more drinks perday), marital status (not married or married), current aspirinuse (use or nonuse), a crude index of fat consumption (estimatedgrams per week for 20 food items, with the participants dividedinto three roughly equal groups),25 and vegetable consumption(the frequency per week of consumption of nine vegetables —not including potatoes — with participants divided intothree roughly equal groups), and status with respect to estrogen-replacementtherapy in women (never used, currently used, or formerly used).
Statistical Analysis
Age-adjusted death rates were calculated for each category ofbody-mass index and were directly standardized to the age distributionof the entire male or female study population. Relative risks(the age-adjusted death rate in a specific body-mass-index categorydivided by the corresponding rate in the reference category[18.50 to 24.99]) were computed; the 95 percent confidence intervalsused approximate variance formulas.26,27
We also used Cox proportional-hazards modeling28 to computerelative risks and to adjust for other potential risk factorsreported at base line. The Cox models were stratified accordingto age at enrollment by the inclusion of age (in single years)in the strata statement of the Cox model. The relative riskswe report are from the multivariate Cox models, unless otherwisenoted. Tests of linear trend were performed by scoring the categoriesof body-mass index, entering the score as a continuous termin the regression model, and testing the significance of theterm by the Wald chi-square test.29
We present results for all cancers combined and for cancer ateach site on the basis of analyses of the total populationsof men and women. For most individual cancer sites, the associationof body-mass index and mortality was similar whether the analysiswas based on the total population or on the population of thosewho had never smoked. However, for several cancers known tobe related to smoking, the association between body-mass indexand mortality was substantially different in the total populationand the population of those who had never smoked. For thesecancers (in men, all cancers, lung cancer, esophageal cancer,pancreatic cancer, and other cancers; in women, all cancers,lung cancer, esophageal cancer, and other cancers), the resultsfrom the population of those who had never smoked are also presented.
Because weight is a modifiable risk factor, we calculated thepopulation attributable fraction (also termed population attributablerisk, population attributable–risk proportion, and excessfraction),30 an estimate of the proportion of all cancer deathsin the United States that might be avoided if the adult populationmaintained a body-mass index in the normal range. We used methodsderived by Walter31 and presented by Kleinbaum et al.32 fora multiple-category exposure. In this analysis, calculationswere based on the multivariate-adjusted relative risks for thetotal population in the Cancer Prevention Study II and for thepopulation of those in that study who had never smoked and onprevalence estimates of overweight and obesity in U.S. men andwomen 50 to 69 years of age from the National Health and NutritionExamination Survey for 1999–2000.33This calculation assumesthat the relative-risk estimates associated with overweightand obesity that were observed in the current study were causaland are generalizable to the U.S. population.
Results
Body-Mass Index and Mortality from Cancer in the Total Population of Men and Women
The numbers of deaths among men were sufficient to permit onlythe death rates from all cancers to be examined separately forthe two highest body-mass-index categories of 35.0 to 39.9 and40.0 or more. The relative risks of death for these categories,as compared with the group of men of normal weight (body-massindex, 18.5 to 24.9), were 1.20 (95 percent confidence interval,1.08 to 1.34) and 1.52 (95 percent confidence interval, 1.13to 2.05), respectively (Table 1). We observed significant positivelinear trends in death rates with increasing body-mass indexfor all cancers, esophageal cancer, stomach cancer, colorectalcancer, liver cancer, gallbladder cancer, pancreatic cancer,prostate cancer, kidney cancer, non-Hodgkin's lymphoma, multiplemyeloma, and leukemia (Table 1). As compared with men of normalweight, men with a body-mass index of at least 35.0 had significantlyelevated relative risks of death from cancer, which ranged from1.23 (95 percent confidence interval, 1.11 to 1.36) for deathfrom any cancer to 4.52 (95 percent confidence interval, 2.94to 6.94) for death from liver cancer (Table 1). In the totalpopulation of men, a significant inverse association was observedbetween body-mass index and death from lung cancer. We did notfind significant associations between body-mass index and deathfrom brain cancer, bladder cancer, melanoma, or "other" cancers.Among men within the normal weight range, those with a body-massindex of 23.0 to 24.9 were not at higher risk for death fromcancer than the leanest men (those with a body-mass index of18.5 to 22.9), and the observed associations in men were notlarger when a leaner group of men was used as the referencegroup (data not shown).
Table 1. Mortality from Cancer According to Body-Mass Index among U.S. Men in the Cancer Prevention Study II, 1982 through 1998.
The results for the total population of women were similar.Women with a body-mass index of at least 40.0 had a relativerisk of death from any cancer of 1.62 (95 percent confidenceinterval, 1.40 to 1.87), as compared with women of normal weight(Table 2). Significant positive linear trends in death rateswere observed for colorectal cancer, liver cancer, gallbladdercancer, pancreatic cancer, breast cancer, cancer of the corpusand uterus, not otherwise specified, cervical cancer, ovariancancer, kidney cancer, non-Hodgkin's lymphoma, multiple myeloma,and "other" cancers (Table 2). The highest relative risk weobserved was for death from uterine cancer (relative risk, 6.25for women with body-mass index of at least 40.0; 95 percentconfidence interval, 3.75 to 10.42). As in men, a significantinverse association between body-mass index and death from lungcancer was seen in the total population, which included smokers.Significant associations with body-mass index were not observedfor death from esophageal cancer, stomach cancer, melanoma,bladder cancer, brain cancer, or leukemia. Although the resultsfor total cancer mortality in women were virtually unchangedwhen a leaner reference group was used (body-mass index, 18.5to 22.9), there were significant differences within the normalweight range for cancers of the gallbladder, breast, and corpusand uterus, resulting in larger elevations in risk for thesecancers throughout the entire range of overweight and obesityas compared with the leanest reference group (the relative riskof death from gallbladder cancer for a body-mass index of atleast 30.0 was 2.44 [95 percent confidence interval, 1.73 to3.44]; the relative risks of death from breast and uterine cancersfor a body-mass index of at least 40.0 were 2.32 [95 percentconfidence interval, 1.54 to 3.50] and 6.87 [95 percent confidenceinterval, 4.09 to 11.55], respectively).
Table 3. Mortality from Cancer According to Body-Mass Index among U.S. Men and Women in the Cancer Prevention Study II Who Had Never Smoked, 1982 through 1998.
As in men, the positive association between body-mass indexand death from any cancer, esophageal cancer, and "other" cancersbecame stronger when the analysis was restricted to women whohad never smoked, and the seemingly protective effect of highbody-mass index on mortality from lung cancer was attenuated(Table 3). Among women who had never smoked, the relative riskof death from any cancer was 1.88 (95 percent confidence interval,1.56 to 2.27) for those with a body-mass index of at least 40.0,as compared with women of normal weight.
The relative risks of cancers for which we found significanttrends of increasing death rates with increasing body-mass indexare summarized for the highest categories of body-mass indexthat we were able to examine in men (Figure 1) and women (Figure 2).
Figure 1. Summary of Mortality from Cancer According to Body-Mass Index for U.S. Men in the Cancer Prevention Study II, 1982 through 1998.
For each relative risk, the comparison was between men in the highest body-mass-index (BMI) category (indicated in parentheses) and men in the reference category (body-mass index, 18.5 to 24.9). Asterisks indicate relative risks for men who never smoked. Results of the linear test for trend were significant (P0.05) for all cancer sites.
Figure 2. Summary of Mortality from Cancer According to Body-Mass Index for U.S. Women in the Cancer Prevention Study II, 1982 through 1998.
For each relative risk, the comparison was between women in the highest body-mass-index (BMI) category (indicated in parentheses) and women in the reference category (body-mass index, 18.5 to 24.9). Asterisks indicate relative risks for women who never smoked. Results of the linear test for trend were significant (P0.05) for all cancer sites.
Population Attributable Fraction
We estimated the proportion of all deaths from cancer in theU.S. population that are attributable to overweight and obesityto be from 4.2 percent to 14.2 percent among men and from 14.3percent to 19.8 percent among women (Table 4). The lower estimatesare based on relative risks for the entire population, whereasthe higher estimates are based on relative risks for those whonever smoked. The estimates based on relative risks among menand women who never smoked (Table 4) do not describe the fractionof deaths attributable to overweight and obesity among thispopulation only. Rather, they are estimates of the fractionof deaths attributable to overweight and obesity in the totalU.S. population, on the assumption that the relative risks amongthose who never smoked offer the most valid estimates of thetrue effect of overweight and obesity on mortality from cancer.
Table 4. Estimated Population Attributable Fraction According to Body-Mass Index for Mortality from Cancer in U.S. Men and Women.
Discussion
The heaviest men and women (those with a body-mass index ofat least 40.0) in the large cohort we studied prospectivelyhad death rates from all cancers that were 52 percent and 62percent higher, respectively, than the rates in men and womenof normal weight. This finding is consistent with those of previousstudies, but the magnitude of the effect is somewhat larger.7,16,17The stronger associations we found probably reflect our abilityto examine deaths from cancer across a wider range of overweightand obesity than has been possible previously. It is also likelythat the stronger associations seen in our study reflect a greatereffect of body-mass index on mortality than on incidence ofcancer at some sites.18,19 These risk estimates are probablyconservative, since they are based on the total population,including current and former smokers. Among women who neversmoked, the relative risk associated with a body-mass indexof at least 40.0 was 88 percent; however, there were not enoughdeaths among men in this category for us to determine the relativerisk.
The International Agency for Research on Cancer (IARC) has concludedthat there is sufficient evidence of a cancer-preventive effectof avoidance of weight gain for cancers of the colon, breast(in postmenopausal women), endometrium, kidney (renal-cell carcinoma),and esophagus (adenocarcinoma).11Potential biologic mechanismsinclude increased levels of endogenous hormones (sex steroids,insulin, and insulin-like growth factor I) associated with overweightand obesity and the contribution of abdominal obesity to gastroesophagealreflux and esophageal adenocarcinoma.11 Our study supports theconclusion of the IARC. Moderate relative risks (less than 2.0)associated with overweight and obesity both for colon cancerand for breast cancer in postmenopausal women have been documentedconsistently in case–control and cohort studies.8,34,35Much higher relative risks have been observed for uterine cancer(2 to 10) and kidney cancer (1.5 to 4), and the increased riskof kidney cancer associated with excess weight is higher inwomen than in men in this and most previous studies.8,36,37Increases by a factor of two to three in the risk of adenocarcinomaof the esophagus in association with high body-mass index havebeen reported,13,14 and the magnitude of this association hasbeen found by other investigators to be greater in nonsmokers.13Because we could not examine esophageal cancer according tosubsite, the stronger association observed in participants whohad never smoked may be partly explained by the greater contributionof adenocarcinoma to all esophageal cancer in nonsmokers thanin smokers.14
Recent studies of gallbladder cancer have consistently foundelevated risks for women with a high body-mass index (by a factorof about two) but generally have involved too few cases forthe association to be evaluated in men.7,16,17,38,39 Obesitymay operate indirectly by increasing the risk of gallstones,which, in turn, increase the risk of gallbladder cancer.8
Studies suggest that high body-mass index is associated withapproximately a doubling of the risk of pancreatic cancer inboth men15,40,41 and women15,41 — a result similar toour findings. In contrast, there is no strong support for anassociation between body-mass index and prostate cancer.42,43,44However, some data suggest a slight increase in the risk ofadvanced prostate cancer or death among patients with a highbody-mass index.19,45,46 Positive associations of ovarian cancerwith body-mass index have been found, with relative risks inthe range of 1.5 to 2.0 for the highest body-mass-index categoriesstudied7,47,48,49; however, several studies have not shown anassociation.16,17,50,51
Two studies that examined obesity and liver cancer found anexcess risk in both men and women, with relative risks in therange of 2.0 to 4.016,17 — a result similar to our findings.Our results and those of a prospective study in Sweden16 suggestthat this excess risk is higher among men than among women.Obesity also increases the risk of adenocarcinoma of the gastriccardia,13,14,52 but the data are limited and inconsistent fornoncardia cancers of the stomach.13,52 In an earlier AmericanCancer Society cohort, as in our study, mortality from stomachcancer was associated with body-mass index among men but notamong women.7 This difference may reflect the greater contributionof the cardia to all cases of gastric cancer in men than inwomen. Our results for cervical cancer are also similar to thosein the earlier American Cancer Society cohort,7 whereas theincreased risks observed in two cohorts of hospitalized patientswith a diagnosis of obesity, as compared with the general population,were much smaller than those observed in our study.16,17 Dataare scarce on the relation between hematopoietic cancers andbody-mass index, and the findings have not been consistent.7,16,17,53
Our results are based on data on mortality and reflect the combinedinfluence of body-mass index both on the incidence of cancerand on survival, whereas most of the available literature onsite-specific cancers is based on incidence data. Our resultsmay be influenced by adiposity-related differences in the diagnosisor treatment of cancer, as well as by true biologic effectsof adiposity on survival. For example, adiposity has been shownto be adversely associated with the incidence of breast cancer,survival among women with the disease,54 and stage at diagnosis.55,56These combined effects may explain why the association of body-massindex with mortality from breast cancer in our study cohortis somewhat stronger than those in previous studies of incidentbreast cancer.18
Smoking profoundly alters the relation between body-mass indexand many causes of death. We believe that public health recommendationsregarding optimal body mass are most valid when they are basedon data from studies of persons who have never smoked.5,57,58For smoking-related cancers, the prospective effects of body-massindex on the risk of death among smokers cannot be separatedfrom the prospective effects of smoking — namely, decreasedbody mass and increased risk of death. Previous analyses ofthe Cancer Prevention Study II cohort demonstrated that theapparent inverse association of body-mass index and mortalitydue to lung cancer was incrementally attenuated with increasinglycomplex statistical control for smoking in multivariate models,and it disappeared entirely when the analysis was restrictedto those who had never smoked.59 Thus, for smoking-related cancers,we believe that the estimates of relative risk and populationattributable fraction presented for the total population (Table 1,Table 2, and Table 4) are likely to be underestimates, whereasthose presented for the population of those who never smoked(Table 3 and Table 4) offer the most valid estimates of thetrue effect of overweight and obesity on mortality from thesecancers.
We used self-reported weight and height at study entry to calculatethe body-mass index, a widely used index of weight adjustedfor height.60,61 Although self-reported weight and height arehighly correlated with measured weight and height,62,63,64 thesmall error that exists is generally systematic, with an overestimationof height and an underestimation of weight, especially at higherweights.62,63,64 Thus, our measure of body-mass index probablyunderestimated the true body-mass-index values among overweightpersons. We had no direct measure of adiposity or of lean bodymass and no measure of central adiposity, such as the waist-to-hipratio. We also could not evaluate the effect of weight changeor weight cycling throughout the follow-up period, and we couldnot estimate the extent of misclassification that weight changemight introduce. The associations observed in this study werenot changed in models that excluded deaths in the first twoyears of follow-up.
From the Department of Epidemiology and Surveillance Research, American Cancer Society, Atlanta.
Address reprint requests to Dr. Calle at the American Cancer Society, 1599 Clifton Rd., NE, Atlanta, GA 30329, or at jcalle{at}cancer.org.
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Barrett, S. V., Paul, J., Hay, A., Vasey, P. A., Kaye, S. B., Glasspool, R. M., On behalf of the Scottish Gynaecological Cancer Tr,
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Chen, Y.-C., Giovannucci, E., Kraft, P., J.Hunter, D.
(2008). Sequence variants of elaC homolog 2 (Escherichia coli) (ELAC2) gene and susceptibility to prostate cancer in the Health Professionals Follow-Up Study. Carcinogenesis
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Ohishi, W., Fujiwara, S., Cologne, J. B., Suzuki, G., Akahoshi, M., Nishi, N., Takahashi, I., Chayama, K.
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0.05) for all cancer sites.