Overweight, Obesity, and Mortality in a Large Prospective Cohort of Persons 50 to 71 Years Old
Kenneth F. Adams, Ph.D., Arthur Schatzkin, M.D., Tamara B. Harris, M.D., Victor Kipnis, Ph.D., Traci Mouw, M.P.H., Rachel Ballard-Barbash, M.D., Albert Hollenbeck, Ph.D., and Michael F. Leitzmann, M.D.
Background Obesity, defined by a body-mass index (BMI) (theweight in kilograms divided by the square of the height in meters)of 30.0 or more, is associated with an increased risk of death,but the relation between overweight (a BMI of 25.0 to 29.9)and the risk of death has been questioned.
Methods We prospectively examined BMI in relation to the riskof death from any cause in 527,265 U.S. men and women in theNational Institutes of Health–AARP cohort who were 50to 71 years old at enrollment in 1995–1996. BMI was calculatedfrom self-reported weight and height. Relative risks and 95percent confidence intervals were adjusted for age, race orethnic group, level of education, smoking status, physical activity,and alcohol intake. We also conducted alternative analyses toaddress potential biases related to preexisting chronic diseaseand smoking status.
Results During a maximum follow-up of 10 years through 2005,61,317 participants (42,173 men and 19,144 women) died. Initialanalyses showed an increased risk of death for the highest andlowest categories of BMI among both men and women, in all racialor ethnic groups, and at all ages. When the analysis was restrictedto healthy people who had never smoked, the risk of death wasassociated with both overweight and obesity among men and women.In analyses of BMI during midlife (age of 50 years) among thosewho had never smoked, the associations became stronger, withthe risk of death increasing by 20 to 40 percent among overweightpersons and by two to at least three times among obese persons;the risk of death among underweight persons was attenuated.
Conclusions Excess body weight during midlife, including overweight,is associated with an increased risk of death.
Substantial epidemiologic evidence indicates that obesity, definedby a body-mass index (BMI) (the weight in kilograms dividedby the square of the height in meters) of 30.0 or more, is associatedwith an increased risk of death.1 However, whether overweight(defined by a BMI of 25.0 to 29.9) increases the risk of deathhas not been established.2 A substantial proportion of the U.S.adult population is overweight but not obese3; any associationbetween overweight and mortality might have important clinicaland public health implications.
Reverse causation owing to preexisting chronic disease and inadequatecontrol for smoking status can distort the true relation betweenbody weight and the risk of death, because chronic illness andsmoking are associated with both decreased BMI and an increasedrisk of death.4 Possible approaches to addressing these potentialbiases include disregarding deaths occurring in the initialperiod of follow-up and restricting the analysis to personswithout preexisting disease or those who have never smoked.Another approach is to evaluate BMI earlier in life,5 when itreflects typical adult weight largely unaffected by the onsetof chronic disease. We examined the association between BMIand the risk of death in the National Institutes of Health (NIH)–AARPDiet and Health Study,6 which is based on a cohort of more thanhalf a million people who were 50 to 71 years old at baseline.At baseline this cohort was large enough to permit the use ofrestriction to minimize potential bias caused by preexistingdisease and smoking. In addition, because information was availableon subjects' weight at the age of 50 years, we were able toanalyze the relation between BMI in midlife and the subsequentrisk of death.
Methods
Study Population
The NIH–AARP Diet and Health Study was established in1995–1996 when 567,169 questionnaires eliciting informationon demographic and anthropometric characteristics, dietary intake,and numerous health-related behavioral patterns were returnedby 18 percent of AARP members who were 50 to 71 years old andresided in six U.S. states (California, Florida, Louisiana,New Jersey, North Carolina, and Pennsylvania) and two metropolitanareas (Atlanta and Detroit).6 We excluded records from 179 personswith duplicate representation in our database; 321 persons whomoved out of the study area; 261 persons who died before theirquestionnaires were received; 15,760 persons whose questionnaireswere completed by a spouse or other surrogate respondent; 16,649,4648, and 2085 persons with missing or extreme values for currentheight or weight, energy intake, or alcohol consumption, respectively;and 1 person who withdrew from the study. We analyzed the datafrom the remaining 527,265 participants (313,047 men and 214,218women).
Follow-up
The vital status of cohort members was determined from 1995–1996through December 31, 2005. Vital status was ascertained by annuallinkage of the cohort to the Social Security AdministrationDeath Master File on deaths in the United States,7 with themost recent update on January 15, 2006. The design and maintenanceof this cohort have been described elsewhere.6,8 The NIH–AARPDiet and Health Study was approved by the Special Studies InstitutionalReview Board of the National Cancer Institute. All participantsprovided written informed consent. All authors vouch for theaccuracy of the data and concur with the interpretation of theresults.
Assessment of Height, Weight, and Other Potential Risk Factors
Information on current height and weight, disease history, smokinghabits, race or ethnic group, physical activity, and diet wascollected by means of a self-administered, mailed questionnaire.The height and weight were used to calculate the BMI, whichwe divided into 10 categories (16.0 to 18.4, 18.5 to 20.9, 21.0to 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 34.9, 35.0 to 39.9, and 40.0 or more) that incorporatedthe definitions of underweight (less than 18.5), normal weight(18.5 to 24.9), overweight (25.0 to 29.9), and obesity (30.0or more) proposed by the World Health Organization classification.9In a subanalysis, we calculated BMI in the cohort at the ageof 50 years on the basis of recalled weight at that age froma supplementary questionnaire mailed to the entire cohort sixmonths after baseline (rate of response, 60 percent).6
Statistical Analysis
Age-adjusted mortality rates were calculated by direct standardization10with the use of five-year age categories. Age-adjusted and multivariaterelative risks were estimated by Cox regression analysis withage as the underlying time metric.11 Multivariate models wereadjusted for race or ethnic group, level of education, smokingstatus, physical activity, and alcohol consumption. We performedstratified analyses to assess whether the association betweenBMI and the risk of death varied according to race or ethnicgroup, age group, smoking status, presence or absence of chronicdisease, and duration of follow-up. We also evaluated the relationsbetween body-mass index and the risk of death according to sexand smoking status with nonparametric regression curves thatused restricted cubic spline12 graphs.
We calculated the population attributable risk,13 which is anestimate of the percentage of premature deaths in the cohortthat would not have occurred if all persons had been of normalweight at the age of 50 years, given the assumption of a causalassociation between weight and the risk of death. Because therelation of BMI to the risk of death differed between currentor former smokers and those who had never smoked, we calculatedthe population attributable risk according to sex both for theentire cohort and for the subgroup of subjects who had neversmoked. The analysis was adjusted for confounding factors andmodification of effects according to age.
Results
During a maximum follow-up of 10 years (4,821,757 person-years),42,173 men and 19,144 women died. As compared with men and womenin the reference group (BMI, 23.5 to 24.9), overweight and obesemen and women had a lower percentage of current smokers, a lowerlevel of education, and were less physically active (Table 1).
Table 1. Baseline Characteristics of 527,265 Men and Women According to BMI.
Among all men (Table 2 and Figure 1A) and women (Table 3 andFigure 2A), including smokers and those with preexisting disease,there was a U-shaped relation between current BMI and the riskof death, with the highest risk in the lowest and the highestcategories of BMI. Overweight was not associated with an increasedrisk of death among men but was weakly associated with an increasedrisk of death among women. The associations between obesityand the risk of death were slightly stronger among Hispanicmen and women and among Asian, Pacific Islander, or Native Americanmen and women than among white or black men and women. The elevatedrisks associated with both extremely high and extremely lowvalues of BMI declined slightly with increasing age in bothmen and women (Table 2 and Table 3 and Figure 1B and Figure 2B).In analyses stratified according to smoking status, we observedstronger associations between obesity and an increased riskof death among those who had never smoked than among formerand current smokers. Underweight was most strongly associatedwith an increased risk of death among former and current smokers(Table 2 and Table 3 and Figure 1C and Figure 2C).
Figure 1. Multivariate Relative Risks of Death in Relation to BMI among Men.
In each panel, the lines are natural cubic splines showing the shape of the dose–response curve for mortality according to BMI on a continuous basis. Relative risks are indicated by solid lines, and 95 percent confidence intervals by dashed lines. Panels A, B, and C are based on current BMI values, whereas Panel D represents BMI at the age of 50 years. The reference point is the midpoint of the reference group (BMI, 23.5 to 24.9) for categorical analyses, with knots placed at the 5th, 25th, 75th, and 95th percentiles of the BMI distribution among all men. The graphic display is truncated at 1 percent and 99 percent of BMI on the basis of the distribution of baseline (current) BMI among all men (Panels A, B, and C) and BMI at the age of 50 years among men who had never smoked (Panel D). All models are adjusted for age, race or ethnic group, level of education, alcohol consumption, and physical activity. The model for all men is adjusted for smoking status and the number of cigarettes smoked per day. The models for men who were former or current smokers are adjusted for the number of cigarettes smoked per day; men for whom information on the number of cigarettes smoked per day was missing were excluded.
Figure 2. Multivariate Relative Risks of Death in Relation to BMI among Women.
In each panel, the lines are natural cubic splines showing the shape of the dose–response curve for mortality according to BMI on a continuous basis. Relative risks are indicated by solid lines, and 95 percent confidence intervals by dashed lines. Panels A, B, and C are based on current BMI, whereas Panel D represents BMI at the age of 50 years. The reference point is the midpoint of the reference group (BMI, 23.5 to 24.9) for categorical analyses, with knots placed at the 5th, 25th, 75th, and 95th percentiles of the BMI distribution among all women. The graphic display is truncated at 1 percent and 99 percent of BMI on the basis of the distribution of baseline (current) BMI among all women (Panels A, B, and C) and BMI at the age of 50 years among women who had never smoked (Panel D). All models are adjusted for age, race or ethnic group, level of education, alcohol consumption, and physical activity. The model for all women is adjusted for smoking status and the number of cigarettes smoked per day. The models for women who were former or current smokers are adjusted for the number of cigarettes smoked per day; women for whom information on the number of cigarettes smoked per day was missing were excluded.
To address the potential effect of bias owing to preexistingdisease and disease-related weight loss, we conducted separateanalyses for participants with and those without preexistingchronic conditions at enrollment (Table 2 and Table 3). We alsodivided the follow-up into earlier and later periods. In bothmen and women, the relation of obesity to the risk of deathwas consistently stronger among participants without preexistingchronic disease than among those with preexisting chronic disease.In separate analyses of the first five years of follow-up andthe subsequent five years of follow-up, the association betweenobesity and the risk of death was stronger in the second thanin the first follow-up period.
We also examined relations between BMI and the risk of deathwithin racial or ethnic groups and age categories after restrictingthe analysis to those without preexisting disease who had neversmoked. These relations within each age group were similar tothose from the age-stratified analyses in the full cohort (datanot shown). The number of deaths among nonwhites was insufficientto allow firm conclusions to be drawn about the relations betweenBMI and the risk of death among those who had never smoked andwere free of preexisting disease.
The prevalence of chronic conditions increased markedly withage: the percentages of participants who reported physician-diagnosedheart disease, emphysema, stroke, end-stage renal disease, orcancer were 13.9 percent among men and women who were 50 to55 years of age at enrollment, 19.2 percent among those 56 to60 years of age, 26.2 percent among those 61 to 65 years ofage, and 33.1 percent among those 66 to 71 years of age. Amongboth men and women 65 years of age or older, weight loss afterthe age of 50 years was more strongly associated with the riskof death than was weight gain (data not shown).
We attempted to correct for potential bias from disease-relatedweight loss by using participants' recalled weight at the ageof 50 years to examine the relation of BMI to the risk of death,after confirming that the association between current BMI andthe risk of death in the subcohort of respondents to the supplementalquestionnaire was consistent with that for the entire cohort(data not shown). In addition, we confirmed that persons classifiedas overweight or obese at baseline who died by the end of thefollow-up period were as likely to respond to the supplementalquestionnaire as their counterparts of normal weight (the responserates were 54.5 percent and 55.9 percent, respectively).
We observed a J-shaped relation between BMI at the age of 50years and the risk of death in both men and women, with a trendtoward increased risk across the entire range of overweightand obese categories (Table 4). In contrast, the relation ofunderweight to the risk of death on the basis of BMI at theage of 50 years was weaker in both men and women than that notedin analyses based on current BMI.
Table 4. Relative Risk of Death in Relation to BMI at the Age of 50 Years among Men and Women.
When we further restricted the analysis of BMI at the age of50 years to participants who had never smoked, we observed significantincreases in the risk of death throughout the range of above-normalcategories of BMI in both men and women (Table 4 and Figure 1Dand Figure 2D). As compared with men with a BMI of 23.5 to 24.9at the age of 50 years, morbidly obese men (BMI of 40.0 or more)had a multivariate relative risk of death of 3.82 (95 percentconfidence interval, 2.87 to 5.08). The corresponding relativerisk among women was 3.79 (95 percent confidence interval, 3.06to 4.70). The increased risk of death among underweight participantsremained but was diminished and not significant, with only 18underweight men and 32 underweight women who died (Table 4).
Excess weight accounted for approximately 7.7 percent of allpremature deaths among men and 11.7 percent of all prematuredeaths among women in the overall cohort. It accounted for 18.1percent of all premature deaths among men who had never smokedand 18.7 percent of all premature deaths among women who hadnever smoked.
Discussion
In this large prospective study, obesity was strongly associatedwith the risk of death in both men and women in all racial andethnic groups and at all ages. After we accounted for potentialbias owing to preexisting disease and residual confounding bysmoking status by using midlife BMI values and restricting theanalysis to participants who had never smoked, we found thateven moderate elevations in BMI conferred an increased riskof death. The risk among participants who were overweight atthe age of 50 years was 20 to 40 percent higher than that amongparticipants who had a BMI of 23.5 to 24.9 at that age. Therisk among obese subjects was two to at least three times thatof participants with a BMI of 23.5 to 24.9. The risk of deathamong underweight participants was attenuated.
Excess body fat has long been recognized as a harbinger of diseaseand early death.14 Nearly a half-century ago, insurance recordsshowed that life expectancy was diminished in obese persons.15Epidemiologic studies subsequently confirmed the link betweenobesity and an increased risk of death.1 Several studies showedthat after smokers and those who died in the early years offollow-up were excluded, above-normal weight (BMI greater than25.0), including overweight, was associated with an increasedrisk of death from any cause.16,17,18,19,20,21,22,23,24
However, whether moderate elevations in BMI (i.e., overweight)truly increase the risk of death is controversial.2 Severalstudies reported no increase in the risk of death among overweightsubjects even after those who died during the initial yearsof follow-up were excluded or subjects were stratified accordingto smoking status.25,26,27,28,29 Recently, Flegal et al. reportedthat overweight was not associated with an excess risk of deathin the nationally representative samples of U.S. adults drawnfrom the National Health and Nutrition Examination Survey.29They speculated that possible causes for their finding mightbe improved medical management of obesity-related chronic diseaseor differences between the U.S. general population and populationsin other studies.29 Others have suggested that inadequate controlfor the combined effects of smoking and chronic illnesses couldbe the explanation.30 Smoking is associated with both a lowerBMI and an increased risk of death and can therefore distortthe relation between BMI and the risk of death. Statisticaladjustment for smoking status does not fully address the problem;the adjusted findings represent a potentially complex combinationof the associations between BMI and the risk of death amongcurrent smokers, former smokers, and those who have never smoked.Restriction of analyses to persons who have never smoked isa powerful tool for addressing this potential bias. Our cohortincluded more than 186,000 men and women who had never smoked.When we restricted our analyses to these persons, the relationof obesity to the risk of death was substantially strengthened,and significant increases emerged in the risk of death, evenamong overweight participants.
Preexisting disease is linked to both decreased weight and anincreased risk of death. Bias related to preexisting diseasecan be circumvented by restricting the analysis to healthy subjectsand excluding those who died during the first years of follow-up(when deaths are more likely to reflect preexisting disease).In our data, the association between overweight or obesity andthe risk of death among both men and women was strengthenedby the use of these techniques.
An alternative approach to addressing bias related to preexistingdisease is to examine weight at an earlier age (50 years inour study), a time of life reflecting typical adult weight andlargely unaffected by the onset of diagnosed disease. When weanalyzed BMI at the age of 50 years in relation to the riskof death, the results were stronger than those based on thecurrent BMI after the exclusion of participants who died duringthe early years of follow-up. This suggests that within the10-year time frame of our study, using weight at a younger agewas more effective in accounting for preexisting disease thanusing current BMI and excluding participants who died duringthe initial years of follow-up. Finally, we observed the strongestassociations between BMI and the risk of death when we combinedanalytic techniques for addressing bias from both preexistingdisease and smoking by examining the relation of adiposity tothe risk of death using BMI at the age of 50 years among thosewho had never smoked.
Large prospective studies are especially valuable for determininga more precise dose–response gradient for the connectionbetween BMI and the risk of death. Our large cohort enabledus to estimate risks of death according to narrow categoriesof BMI with great precision and to discern not only an elevatedrisk for most categories of overweight but also substantiallyenhanced risk among the obese.
Although we did not compare our participants' assessments ofheight and weight with directly measured values, self-reportedheight and weight are generally known to be accurate. The correlationbetween BMI based on self-reported height and weight and thatbased on measured height and weight is typically greater than0.9,31 and weight recalled from 28 years previously by elderlypeople has been reported to have a correlation of more than0.8 with measured weight at that time.32 Some evidence suggeststhat obese persons are more likely to underestimate their weightthan are persons of normal weight.33 This bias may be offsetif underweight persons at higher risk for death report normalweight and are thus misclassified in the reference group. Onbalance, and given the strong correlation between self-reportedand measured weight, including weight at the age of 50 years,the combined effect of random and systematic reporting erroron the observed association between BMI and the risk of deathis probably minimal.
We adjusted for several variables, including level of education,race or ethnic group, alcohol consumption, and physical activity,which allowed us to minimize the potential for confounding bythese factors. Because we cannot rule out the possibility thatunmeasured or unknown confounding factors accounted for theassociations observed in our study, we cannot conclude withcomplete certainty that the relation between adiposity and therisk of death is causal.
The biomedical foundation for an association between excessbody fat and the risk of death is well established. Medicalcomplications of adiposity include hypertension, type 2 diabetesmellitus, cardiovascular disease, pulmonary disease, and cancer.34Pathophysiologic processes that could plausibly mediate theconnection between BMI and the risk of death include insulinresistance, lipid abnormalities, hormonal alterations, and chronicinflammation.35,36
The NIH–AARP Diet and Health Study is a contemporary investigationwith vital status ascertained from 1995–1996 through theend of 2005. Many of the participants, who were 50 to 71 yearsold at baseline, are from the baby-boomer generation. Much hasbeen written recently about the rise in obesity — andits medical consequences — in this segment of the population.37,38Even against the background of advances in the management ofobesity-related chronic diseases in the past few decades, ourfindings suggest that adiposity, including overweight, is associatedwith an increased risk of death.
Supported by the Intramural Research Program of the NationalCancer Institute, National Institutes of Health.
No potential conflict of interest relevant to this article wasreported.
The views expressed are those of the authors.
We are indebted to the participants in the NIH–AARP Dietand Health Study for their outstanding cooperation, to Dr. AnneThiebaut for statistical advice, and to Leslie Carroll and DavidCampbell at Information Management Services and Tawanda Royat the Nutritional Epidemiology Branch for research assistance.
Source Information
From the Nutritional Epidemiology Branch (K.F.A., A.S., T.M., M.F.L.), Division of Cancer Epidemiology and Genetics and the Biometry Research Group (V.K.), Division of Cancer Prevention, and the Division of Cancer Control and Population Sciences (R.B.-B.), National Cancer Institute, and the Laboratory of Epidemiology, Demography, and Biometry, National Institute on Aging (T.B.H.), the National Institutes of Health, Bethesda, Md.; and the AARP, Washington, D.C. (A.H.).
Address reprint requests to Dr. Adams at the Nutritional Epidemiology Branch, 6120 Executive Blvd., Suite 320, Rockville, MD 20852, or at adamske{at}mail.nih.gov.
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Overweight, Obesity, and Mortality
Appels C. W.Y., Vandenbroucke J. P., Hoofnagle J. H., Barzel U. S., Spitzer J., Adams K. F., Schatzkin A., Leitzmann M. F.
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355:2699-2701, Dec 21, 2006.
Correspondence
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