Background Body-mass index (the weight in kilograms dividedby the square of the height in meters) is known to be associatedwith overall mortality. We investigated the effects of age,race, sex, smoking status, and history of disease on the relationbetween body-mass index and mortality.
Methods In a prospective study of more than 1 million adultsin the United States (457,785 men and 588,369 women), 201,622deaths occurred during 14 years of follow-up. We examined therelation between body-mass index and the risk of death fromall causes in four subgroups categorized according to smokingstatus and history of disease. In healthy people who had neversmoked, we further examined whether the relation varied accordingto race, cause of death, or age. The relative risk was usedto assess the relation between mortality and body-mass index.
Results The association between body-mass index and the riskof death was substantially modified by smoking status and thepresence of disease. In healthy people who had never smoked,the nadir of the curve for body-mass index and mortality wasfound at a body-mass index of 23.5 to 24.9 in men and 22.0 to23.4 in women. Among subjects with the highest body-mass indexes,white men and women had a relative risk of death of 2.58 and2.00, respectively, as compared with those with a body-massindex of 23.5 to 24.9. Black men and women with the highestbody-mass indexes had much lower risks of death (1.35 and 1.21),which did not differ significantly from 1.00. A high body-massindex was most predictive of death from cardiovascular disease,especially in men (relative risk, 2.90; 95 percent confidenceinterval, 2.37 to 3.56). Heavier men and women in all age groupshad an increased risk of death.
Conclusions The risk of death from all causes, cardiovasculardisease, cancer, or other diseases increases throughout therange of moderate and severe overweight for both men and womenin all age groups. The risk associated with a high body-massindex is greater for whites than for blacks.
The relation between body weight and mortality remains controversial.Important unresolved questions concern the shape of the curverelating the two variables; the optimal weight for longevity;whether the optimal weight varies according to age, race, orsex; and whether the increased death rates often observed amongvery lean people are causal or an artifact of leanness due tosmoking or concurrent illness. Debate about the potential hazardsof excessive leanness has received disproportionate attentionin a culture in which obesity is far more prevalent.
Much of the vast literature examining the relation between bodyweight and mortality1,2,3,4,5,6,7,8,9,10,11,12,13,14,15,16 supportsthe hypothesis of a curvilinear relation, in which the riskis increased among the very heavy and the very lean. However,many of the studies that found increased risk to be associatedwith leanness have been criticized17,18 for failing to excludesmokers and people with concurrent illness. Several prospectivestudies that excluded smokers and those with existing diseasehave challenged the notion of a curvilinear relation, suggestingthat, overall, death rates increase linearly with increasingadiposity, with no excess risk among the very lean.8,10,12,15
Other areas of controversy pertain to whether the optimal weightfor longevity increases with age or varies according to race.Past weight guidelines have recommended a higher maximal weight(for height) with increasing age.19 There is disagreement, however,as to whether this practice is justified18; the Department ofAgriculture's 1995 Dietary Guidelines for Americans20 did notinclude age-specific recommendations. Contributing to the controversyare the findings that the relative risk of death associatedwith adiposity decreases with increasing age3,10,11,14,15 andthat the optimal weight for longevity may be higher in olderpopulations.1,2,13 Although relatively few cohort studies haveexamined the effects of adiposity on mortality among blacks,2,4,21,22,23,24,25,26the available literature suggests that adiposity may be a lessimportant predictor of mortality among blacks than among whites,particularly among women.
To investigate further the risk of death associated with bodyweight in men and women and to determine whether this risk variesaccording to smoking and disease status, race, cause of death,and age, we examined the association between body-mass indexand death rates in a large, prospective cohort of U.S. adults.
Methods
Study Population
The study subjects were selected from the 1,184,657 participantsin the Cancer Prevention Study II, a prospective study of mortalityamong men and women in the United States that was begun by theAmerican Cancer Society in 1982.27 Participants were identifiedand enrolled by more than 77,000 volunteers in all 50 states,the District of Columbia, and Puerto Rico. Families were enrolledif at least one household member was 45 years of age or older,and all enrolled members were at least 30 years old. The averageage of the participants at enrollment was 57 years. In 1982,the participants completed a confidential questionnaire thatwas mailed to them; they provided information on demographiccharacteristics, personal and family history of cancer and otherdiseases, various aspects of behavior, environmental and occupationalexposures, and diet.
Deaths that occurred between the month of enrollment and December31, 1996, were ascertained through personal inquiries by volunteersin September 1984, September 1986, and September 1988 and thenthrough linkage with the National Death Index.28 As of December31, 1996, a total of 20.1 percent of the participants had died,79.7 percent were still living, and 0.2 percent had had follow-uptruncated on September 1, 1988, because of insufficient datafor linkage with the National Death Index. Death certificatesor codes for cause of death were obtained for 98.6 percent ofall deaths.
In the questionnaire, participants were asked to give theircurrent weight, weight one year previously, and height (withoutshoes). We excluded from the analysis participants with extremevalues for height or weight (those at or below the 0.1 percentileand those at or above the 99.9 percentile) or for whom thesevalues were not known. In addition, we excluded participantsfor whom we did not have information on race or who were notwhite or black. We also excluded participants for whom smokingstatus and prior weight were unknown. After these exclusions,457,785 men and 588,369 women were eligible for participationin our study. A total of 113,517 men and 88,105 women in thispopulation died during the 14 years of follow-up.
Body-Mass Index
We categorized body-mass index (the weight in kilograms dividedby the square of the height in meters), which we used as ourmeasure of adiposity, as lower than 18.5, 18.5 to 20.4, 20.5to 21.9, 22.0 to 23.4, 23.5 to 24.9, 25.0 to 26.4, 26.5 to 27.9,28.0 to 29.9, 30.0 to 31.9, 32.0 to 34.9, 35.0 to 39.9, and40.0 or higher. We created these 12 categories to allow a detailedexamination of the association between body-mass index and mortalityacross a wide range of body-mass values without a priori assumptionsabout the shape of the dose–response curve. In addition,combinations of these categories correspond to the cutoff pointsproposed by the World Health Organization for what it termsthe normal range (a body-mass index between 18.5 and 24.9),grade 1 overweight (between 25.0 and 29.9), grade 2 overweight(between 30.0 and 39.9), and grade 3 overweight (40.0 or higher).29
End Points
Death from all causes was the primary end point in these analyses.In addition, we examined the association between body-mass indexand death due to cardiovascular disease (codes 390 through 459of the International Classification of Diseases, Ninth Revision[ICD-9]), cancer (ICD-9 codes 140 through 208), and all othercauses.30
Subgroups
From the cohort of 1,046,154 men and women, we established fourmutually exclusive subgroups categorized according to smokingstatus and history of disease — current or former smokerswith a history of any of the following: cancer (but not nonmelanomaskin cancer), heart disease, stroke, respiratory disease (chronicbronchitis, emphysema, or asthma), current illness (of any type),or a weight loss of at least 10 lb (4.5 kg) in the previousyear; current or former smokers with no history of disease atenrollment; those who had never smoked and who had a historyof disease at enrollment; and those who had never smoked andwho had no history of disease at enrollment (Table 1). For eachof the four subgroups, we examined the association between body-massindex and overall mortality according to sex.
Table 1. Cohorts in the Analysis of Overall Mortality and Body-Mass Index.
In the 81,468 white men, 2908 black men, 208,710 white women,and 9147 black women who had never smoked and had no disease,we further examined whether the association between body-massindex and mortality varied according to race, cause of death,or age. For these analyses, we combined categories of body-massindex, if necessary, to avoid having fewer than 15 deaths ina category.
Statistical Analysis
We calculated age-adjusted death rates for each category ofbody-mass index and standardized these rates to the age distributionof the entire male or female study population. We computed summaryrate ratios (the death rate in a category of body-mass indexdivided by the corresponding rate in the reference category[body-mass indexes between 23.5 and 24.9]) and the rate differences(the death rate in a category minus that in the reference category);we used approximate variance formulas to calculate 95 percentconfidence intervals.31
We also used a Cox proportional-hazards model32 to compute relativerisk and to adjust for other potential risk factors reportedat base line. We adjusted Cox models for exact age at enrollment,level of education and physical activity, alcohol use, maritalstatus, current use of aspirin, a crude index of fat consumption,33vegetable consumption, and (in women) use of estrogen-replacementtherapy. All relative risks are from the multivariate Cox modelsunless otherwise noted.
Results
Effect of Smoking Status and History of Disease
The relation between body-mass index and death from all causesdiffered according to smoking status and the presence or absenceof a history of disease (Figure 1). Obesity was most stronglyassociated with an increased risk of death among those who hadnever smoked and who had no history of disease, whereas leannesswas most strongly associated with an increased risk of deathamong current or former smokers with a history of disease. Forcurrent or former smokers with no history of disease and forthose who had never smoked and who had a history of disease,the pattern was intermediate.
Figure 1. Multivariate Relative Risk of Death from All Causes among Men and Women According to Body-Mass Index, Smoking Status, and Disease Status.
The four subgroups are mutually exclusive. Nonsmokers had never smoked. The reference category was made up of subjects with a body-mass index of 23.5 to 24.9.
The absolute risk of death varied substantially among thesefour subgroups. The age-standardized rates of death from allcauses were lowest among those who had never smoked and whohad no history of disease (at a body-mass index between 23.5and 24.9, there were 962 deaths per 100,000 men per year and682 deaths per 100,000 women per year), highest among currentor former smokers with a history of disease (2896 deaths per100,000 men per year and 1796 deaths per 100,000 women per year),and intermediate among those who were current or former smokerswith no history of disease (1559 deaths per 100,000 men peryear and 1023 deaths per 100,000 women per year) or those whohad never smoked and who had a history of disease (1819 deathsper 100,000 men per year and 1266 deaths per 100,000 women peryear).
Among subjects who had never smoked and who had no history ofdisease, the highest mortality rates were among the heaviestmen (relative risk, 2.68; 95 percent confidence interval, 1.76to 4.08) and women (relative risk, 1.89; 95 percent confidenceinterval, 1.62 to 2.21). There were much smaller increases inrisk among the leanest men (relative risk, 1.28; 95 percentconfidence interval, 1.04 to 1.58) and women (relative risk,1.36; 95 percent confidence interval, 1.26 to 1.48). The nadirof the curve of body-mass index and mortality was at a body-massindex between 23.5 and 24.9 in men and 22.0 and 23.4 in women.Relative risks were not significantly different from 1.00 forthe range of body-mass index between 22.0 and 26.4 in men and20.5 and 24.9 in women.
Effect of Race
Among subjects who had never smoked and who had no history ofdisease the association between a high body-mass index and anincreased risk of death from all causes was stronger in whitesthan in blacks (Table 2). At the highest level of body-massindex, white men and women had relative risks of 2.58 and 2.00,respectively. In contrast, the association between a high body-massindex and an increased risk of death appeared more moderateamong black men (relative risk, 1.35; 95 percent confidenceinterval, 0.89 to 2.06). However, the small numbers of deathsamong black men limited our analysis of risk at very high levelsof body-mass index. In black women, a small (20 to 30 percent)increase in risk was found only at the highest levels of body-massindex (35.0 or higher), and it was not statistically significant.Extreme leanness was associated with some increase in overallmortality in all subgroups (Table 2).
Table 2. Rates and Relative Risks of Death from All Causes among Subjects Who Had Never Smoked and Who Had No History of Disease, According to Body-Mass Index, Race, and Sex.
Effect of Cause of Death
The shape of the mortality curve differed according to the causeof death among subjects who had never smoked and who had nohistory of disease (Figure 2). The relation between body-massindex and the risk of death from cancer was positive and showedno elevation in risk among the leanest persons. The curve forthe risk of death from cardiovascular disease was J-shaped;for the risk of death from all other causes, the curve was U-shaped.The J-shaped and U-shaped curves were explained primarily byan increased risk of death among lean men and women as a resultof cerebrovascular disease, pneumonia, and diseases of the centralnervous system (data not shown). A high body-mass index wasmost predictive of death from cardiovascular disease, especiallyin men (relative risk, 2.90; 95 percent confidence interval,2.37 to 3.56). Significantly increased risks of death from cardiovasculardisease were found at all body-mass indexes of more than 25.0in women and 26.5 in men.
Figure 2. Multivariate Relative Risk of Death from Cardiovascular Disease, Cancer, and All Other Causes among Men and Women Who Had Never Smoked and Who Had No History of Disease at Enrollment, According to Body-Mass Index.
The reference category was made up of subjects with a body-mass index of 23.5 to 24.9.
Effect of Age
A high body-mass index was associated with increased risk ofdeath from all causes at all ages among both men and women whohad never smoked and who had no history of disease (Table 3).Although the relative increase in risk associated with a highbody-mass index declined with increasing age (to a 50 percentincrease in men 75 years of age or older and to a 40 to 50 percentincrease in women 75 or older), the absolute increase in deathrates associated with a high body-mass index was greatest inelderly men and women. The excess risk for the heaviest menand women who were 75 or older, expressed as the differencein rates, was 2230 deaths per 100,000 men per year and 1652deaths per 100,000 women per year. The nadir of the curve waswithin the range of body-mass index from 20.5 to 24.9 for allsix groups categorized according to age and sex.
Table 3. Rates and Relative Risks of Death from All Causes among Subjects Who Had Never Smoked and Who Had No History of Disease, According to Body-Mass Index, Sex, and Age.
Discussion
In this large, prospective study, the lowest rates of deathfrom all causes were found at body-mass indexes between 23.5and 24.9 in men and 22.0 and 23.4 in women; relative risks werenot significantly elevated for the range of body-mass indexesbetween 22.0 and 26.4 in men and 20.5 and 24.9 in women. Deathrates increased throughout the range of moderate and severeoverweight for both men and women, but less so for blacks, particularlyblack women. The risk of death increased with an increasingbody-mass index in all age groups and for all categories ofcauses of death.
As expected,17 the shape and magnitude of the association betweenbody-mass index and mortality were substantially modified bya history of both smoking and disease, factors that are predictiveof leanness and poor survival. Limiting the primary analysesto subjects who had never smoked and who had no history of diseaseat enrollment greatly reduced the apparent elevation in therisk of death among lean persons, increased the risk among heavypersons, and shifted downward the body-mass index level associatedwith the lowest risk of death. Among current or former smokerswith a history of disease, the prospective effect of body-massindex on the risk of illness and death cannot be separated fromthe effect of smoking and disease on the body-mass index. Publichealth recommendations regarding optimal body-mass index aretherefore most valid when they are based on studies of healthypersons who have never smoked.
We found, as did previous studies,2,21,22,23,24,26 that obesitywas least strongly associated with the risk of death from anycause among black women. Among black women, we found a small(approximately 20 to 30 percent) increase in risk for thosewith a body-mass index of 35.0 or higher, in contrast to therisk among the heaviest white women, which was increased byapproximately 75 to 100 percent. Although black women tend tohave a relatively central and abdominal distribution of bodyfat as compared with white women,21,34 some evidence suggeststhat the central distribution of fat in black women may havea weaker effect on atherogenic risk factors such as levels ofcholesterol, triglycerides, and sex hormone–binding globulinand degree of peripheral insulin resistance.34 Our findingsin black men parallel the findings of other studies2,21,26 inshowing moderate (approximately 20 to 35 percent) increasesin mortality at body-mass index levels of 25.0 or higher. However,there were insufficient numbers of black men in our cohort whohad a body-mass index of 32.0 or higher for us to evaluate theeffect of extreme adiposity in these men.
The cause of death modified the relation between body-mass indexand the risk of death in both men and women. The heaviest menand women had a 40 to 80 percent increase in the risk of dyingfrom cancer, and there was no evidence of an increased riskamong the leanest subjects, findings consistent with the resultsof studies in animals that showed that dietary restriction candramatically decrease the incidence of tumors and the rate oftumor growth.35 In contrast to the fairly linear relation foundin the risk of death from cancer, a curvilinear relation wasfound for the risks of death from cardiovascular disease anddeath from other causes. These findings were explained primarilyby an increased risk of death among lean men and women as aresult of cerebrovascular disease, pneumonia, and diseases ofthe central nervous system. In other prospective studies, leannesshas been associated with an increased risk of respiratory disease14and cerebrovascular disease.14,36
A high body-mass index was associated with higher rates of deathfrom all causes among both men and women in all age groups,including those 75 years or older. Although the relative riskof death declined with increasing age, the absolute risk ofdeath associated with adiposity increased substantially withincreasing age and was highest in the oldest age groups. Theseage-specific findings are similar to the recently publishedresults of an earlier study of an American Cancer Society cohort,the Cancer Prevention Study I.15 When we used either absoluteor relative measures of risk, our data indicated that heaviermen and women have an increased risk of death at all ages. Theoptimal body-mass index for longevity fell between 20.5 and24.9 for men and women of all ages. These data offer supportfor the use of a single recommended range of body weight throughoutlife.
Despite our best efforts to control for bias from antecedentdisease, it is likely that we were unable to eliminate suchbias completely. Thus, the increased risk of death from specificcauses that was associated with leanness in this and other studiesmay reflect preexisting, but unrecognized, disease processes,even after careful exclusions have been made. Also, althoughwe had information on recent weight loss, we were unable tocontrol for long-term weight loss. Several investigators havesuggested that there is an association between illness-relatedweight loss over a period of many years and the subsequent riskof death in very thin persons and that controlling for recentweight loss may be insufficient.3,13
Although an understanding of the risk associated with leannessis of scientific interest, in terms of public health, of greaterconcern is the excess risk of death due to obesity. Nearly onethird (32.6 percent) of adults in the United States meet theWorld Health Organization's definition of grade 1 overweight(a body-mass index between 25.0 and 29.9), and 22.3 percentmeet the criteria for grade 2 and grade 3 overweight (a body-massindex of 30.0 or higher).37 In contrast, only 7.7 percent ofadults in the United States have a body-mass index lower than20.0, and only 1.5 percent have a body-mass index lower than18.0.37
The measure of adiposity that we used in our study has severallimitations. We used self-reported weight and height at enrollmentto calculate body-mass index, a widely used37 index of weightadjusted for height. Although self-reported weight and heightare highly correlated with measured weight and height,38 a small,generally systematic, error exists — an overestimationof height and an underestimation of weight, especially at higherweights.38 Thus, our measure of body-mass index probably underestimatedthe true body-mass index of overweight persons (e.g., a body-massindex of 27 calculated from self-reported weight and heightis likely to have been closer to a true value of 28). We hadno direct measure of adiposity or of lean body mass, and wehad no measure of central adiposity, such as the ratio of waistcircumference to hip circumference. Although the body-mass indexis highly correlated with more direct measures of body fat inmost populations,39 it may be a less useful indicator of adiposityamong the elderly, who tend to have a shift of fat from peripheralto central sites with a concomitant increase in waist-to-hipratio but no increase in body-mass index.40 Folsom et al.5 foundthe waist-to-hip ratio to be a better predictor of the riskof death than the body-mass index in a prospective cohort ofolder women in Iowa.
The large size of our cohort allowed us to follow, for a 14-yearperiod, more than 300,000 apparently healthy people who hadnever smoked and to investigate the relation between body-massindex and the risk of death across a wide range of body-mass–indexvalues and according to age, race, sex, and cause of death.In addition, we were able to control for other potential confoundersof the relation.
In summary, our findings support the well-established increasein the risk of death associated with severe overweight as wellas a gradient of increasing risk associated with moderate overweight.The consistency of our findings in men and women and in allage groups also argues for the use of a single recommended rangeof body weight throughout life.
We are indebted to Richard Peto, F.R.S., and Drs. I-Min Lee,Alan D. Lopez, and David F. Williamson for their thoughtfulreview and comments and to Missy Jamison for data managementand collection.
Source Information
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.
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Body-Mass Index and Mortality
Byers T., Durazo-Arvizu R. A., Goldbourt U., McGee D. L., Calle E. E., Thun M. J., Rodriguez C.
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N Engl J Med 2000;
342:286-289, Jan 27, 2000.
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