Association of BMI and Weight Change With All Cause Mortality in Elderly

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Original Contribution

Association of Body Mass Index and Weight Change with All-Cause Mortality

in the Elderly

Mara M. Corrada1,2, Claudia H. Kawas1,2,3, Farah Mozaffar2, and Annlia Paganini-Hill4

1 Department of Neurology, School of Medicine, University of California, Irvine, CA.2 Institute for Brain Aging and Dementia, University of California, Irvine, CA.3 Department of Neurobiology and Behavior, School of Biological Sciences, University of California, Irvine, CA.4 Department of Preventive Medicine, Keck School of Medicine, University of Southern California, Los Angeles, CA.

Received for publication August 22, 2005; accepted for publication December 21, 2005.

The authors explored the relation of body mass index (BMI; weight (kg)/height (m)2) and weight change to all-

cause mortality in the elderly, using data from a large, population-based California cohort study, the Leisure World

Cohort Study. They estimated relative risks of mortality associated with self-reported BMI at study entry, BMI at age

21 years, and weight change between age 21 and study entry. Participants were categorized as underweight (BMI


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the advantage of possessing information on many variablesthat may confound or modify the association betweenweight and mortality.

MATERIALS AND METHODS

Participants

Participants were members of the Leisure World CohortStudy, a population-based study initiated in 1981. A healthquestionnaire was mailed on June 1, 1981, to all residentswho owned homes in Leisure World Laguna Hills, a retire-ment community in California. Residents who moved intothe community after this date were sent surveys in 1982,1983, and 1985. The survey was returned by 13,978 resi-dents (61 percent). Nonrespondents had higher hospitaliza-tion rates than respondents during the first year of follow-upand higher death rates during the first 3 years but not there-after (3). The cohort, like the population, is primarily Cau-casian, educated, and upper middle-class; two thirds are

female. The health questionnaire collected information ondemographic factors, medical history (selected data), exer-cise, and smoking, among other variables. The institutionalreview boards of the University of Southern California andthe University of California, Irvine, approved the study.

Potential predictors of mortality

BMI at study entry and at age 21 years. Participants wereasked to report their height (in inches) and weight (inpounds) at the time of the survey and to estimate theirweight at age 21 years. BMI at study entry was based onself-reported weight and height at entry, and BMI at age 21

was based on self-reported weight at age 21 and height atentry. BMI (weight (kg)/height (m)2) was categorized ac-cording to federal guidelines (4): underweight (5 percent loss,5 percent change (stable), >515 percent gain, and >15percent gain. Participants were then classified into 12 cate-

gories according to their BMI at age 21 and their weightchange from age 21 to study entry. The reference categorywas normal weight at age 21 and stable weight.

Physical activity as a potential confounder. Studies on therelation between BMI and mortality emphasize the impor-tance of adjusting for physical activity given the high degreeof confounding that may occur when studying either factoralone (5). Therefore, we present the results of our analysesboth with and without adjustment for physical activity. Aspart of the survey, participants reported the amount of timethey spent in several activities on an average weekday. Theactivities included active outdoor activities (e.g., swimming,biking, jogging, tennis, vigorous walking) and active indoor

activities (e.g., exercising, dancing). The response catego-ries were 0 minutes, 15 minutes, 30 minutes, 1 hour, 2 hours,34 hours, 56 hours, 78 hours, and 9 or more hours perday. We calculated the amount of time spent per day in activeactivities by summing time spent in active outdoor activitiesand time spent in active indoor activities. Responses weregrouped into seven categories: 0 minutes (reference cate-

gory), 15 minutes, 30 minutes, 45 minutes, 11.75 hours,22.75 hours, and 3 or more hours per day. We selectedcategories before conducting the analyses in order to ensuresufficient numbers of participants in each category. Al-though more passive activities such as fishing, gardening,reading, and crafts were assessed as part of the question-naire, they were not included in the category of active activ-ities analyzed here.

Medical history as a potential confounder. Some authorshave suggested that adjustment for factors such as hyperten-sion, diabetes, and high cholesterol results in biased esti-mates, since these factors are biologic intermediates in thecausal pathway between obesity and mortality rather than

confounders (6, 7). Therefore, we show the results of allanalyses both with and without adjustment for the avail-able medical history variables known to be associated withmortality in our study and others: hypertension, angina,myocardial infarction, stroke, diabetes mellitus, rheuma-toid arthritis, and cancer (excluding skin cancer other thanmelanoma).

Outcome ascertainment

Cohort members have been followed by means of peri-odic resurveys, reviews of local hospital discharge records,and determination of vital status through searches of na-

tional and commercial death indexes and ascertainment ofdeath certificates. Findings presented in this report werebased on follow-up data through December 31, 2004. Asof that date, 51 participants (0.4 percent) had been lost tofollow-up. Further details on the data collection methodsused and the validity of exposure and outcome data areavailable in previously published reports (3, 810).

Statistical analysis

We used Cox regression (11) to estimate the relative riskof all-cause mortality associated with BMI at study entry,BMI at age 21 years, and weight change from age 21 tostudy entry. Participants not known to have died by Decem-

ber 31, 2004, were censored at their age on that date. Allanalyses were adjusted for age at entry (continuous vari-able), gender, and smoking status at entry (never, past, orcurrent smoker). We also present the results of analyses withadjustment for physical activity (seven categories) and med-ical history (positive vs. negative). All analyses were per-formed using SAS software, version 9.1 for Windows (SASInstitute, Inc., Cary, North Carolina).

To address the possibility that the relation between thefactors under study and mortality may have been con-founded by preexisting disease, we repeated the analysesafter excluding the first 5 years of follow-up. To explorepotential differences in the association between BMI and

BMI, Weight Change, and Mortality in the Elderly 939

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mortality according to smoking status, age at entry, andgender, we performed additional stratified analyses.

RESULTS

We analyzed data for 13,451 participants after deleting

527 participants with missing data for the variables of in-terest. Table 1 shows the characteristics of these partici-pants. The average age at study entry was 73 years, theaverage duration of follow-up was 13 years, and the major-ity of participants were women (64 percent). Table 1 alsoshows the characteristics of participants by BMI category atstudy entry. People in the higher BMI categories were youn-ger at entry, had greater weight gain, and were more likely tohave a history of hypertension or diabetes but were lesslikely to smoke or have a history of stroke or cancer.

BMI at study entry

Table 2 shows the relation between BMI at study entry

and all-cause mortality, with adjustment for age at entry,gender, and smoking (model 1). The relation was reverseJ-shaped. Underweight participants had the highest mortal-ity (relative risk (RR) 1.51) in comparison with those inthe normal weight category. Obese participants (RR 1.25)also had increased mortality. Being overweight (RR 1.01)was not associated with excess mortality. Adjustment forphysical activity (model 2) or for physical activity and med-ical history (model 3) slightly attenuated the relative risk forpersons in the obese category (RR 1.12).

In analyses excluding the first 5 years of follow-up, 2,076decedents were excluded (bottom half of table 2). The as-sociation between BMI at study entry and all-cause mortal-

ity, after adjustment for age at entry, gender, and smoking(model 1), was U-shaped. In these analyses, the relative riskfor being underweight was somewhat attenuated (RR 1.39). Adjustment for physical activity (model 2) or forphysical activity and medical history (model 3) attenuatedthe relative risk for obese persons, making the associationonce again reverse J-shaped.

BMI at age 21 years

With adjustment for age at study entry, gender, and smok-ing, all-cause mortality was significantly increased amongparticipants who were overweight/obese at age 21 years(RR 1.17) in comparison with those of normal weightat 21 (table 3, model 1). The mortality risk was not differentfor underweight participants (RR 1.05). Adjustment forphysical activity (model 2) or for physical activity and med-ical history (model 3) resulted in similar risk estimates.Excluding the first 5 years of follow-up had little effect onthe association between BMI at age 21 and all-cause mor-tality (bottom half of table 3).

Weight change

Table 4 shows the relation between all-cause mortalityand weight at age 21 years by weight-change category. Withadjustment for age at entry, gender, and smoking, mortality

was significantly increased for participants who lost weight,regardless of their weight at age 21 (model 1). The relativerisks were 1.93, 1.28, and 1.26 for being underweight, nor-mal weight, and overweight/obese, respectively, at age 21.Mortality was also significantly increased among personswho were underweight at age 21 and remained at a stableweight (RR 1.48) and among persons who were over-

weight/obese at age 21 and gained more than 15 percentof their body weight (RR 1.32). With adjustment forphysical activity and medical history (models 2 and 3), therelative risks were generally similar in magnitude, but thestatistical significance of some risks changed, including sig-nificantly lower mortality with weight gain among personswho were underweight or normal weight at age 21.

The association between weight change and all-causemortality did not change greatly after exclusion of the first5 years of follow-up. With adjustment for all potential con-founders, the main differences were that 1) the relative riskamong persons who were underweight at age 21 and lostweight was attenuated (RR 1.62, 95 percent CI: 1.06,

2.47); 2) the relative risk among persons who were under-weight at age 21 and gained more than 15 percent of theirweight remained similar in magnitude but was no longersignificant (RR 0.94, 95 percent CI: 0.86, 1.03); and3) the relative risk among persons of normal weight at age21 who gained 515 percent of their weight was also similarin magnitude but no longer significant (RR 0.96, 95 per-cent CI: 0.91, 1.03).

Stratification by smoking status

The association between BMI at study entry and all-causemortality varied among the different smoking categories

(figure 1). For never smokers, the association was U-shaped,with similarly increased mortality among both underweight(RR 1.26, 95 percent CI: 1.12, 1.43) and obese (RR 1.35, 95 percent CI: 1.17, 1.57) participants in comparisonwith normal-weight participants. For past smokers, the as-sociation was reverse J-shaped, with the highest mortalitybeing seen among underweight participants (RR 1.81, 95percent CI: 1.54, 2.14), although obese participants also hadincreased mortality (RR 1.19, 95 percent CI: 1.03, 1.38).Among current smokers, underweight participants had in-creased mortality (RR 1.99, 95 percent CI: 1.61, 2.46)while overweight or obese participants did not differ frompersons of normal weight.

Excluding the first 5 years of follow-up slightly changed

the curves for the three smoking categories. The relativerisks among underweight participants in all smoking cate-gories, especially past smokers, were attenuated (neversmokers: RR 1.21, 95 percent CI: 1.05, 1.40; past smok-ers: RR 1.50, 95 percent CI: 1.21, 1.86; current smokers:RR 1.91, 95 percent CI: 1.49, 2.46). Conversely, therelative risk among obese past smokers was slightly in-creased (RR 1.25, 95 percent CI: 1.07, 1.47).

Stratification by age

Figure 2 shows the shape of the association between BMIat study entry and all-cause mortality for four categories of

940 Corrada et al.

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age at entry (


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nonsignificant relative risks being observed among under-weight and obese participants.

Stratification by gender

The curves for the association between BMI at studyentry and all-cause mortality were almost identical for

men and women (not shown). After adjustment for age atentry and smoking, the curves were reverse J-shaped, withunderweight men (RR 1.52, 95 percent CI: 1.21, 1.90) and

women (RR 1.52, 95 percent CI: 1.37, 1.67) having thehighest mortality compared with those in the normal-weightcategory. Obese men (RR 1.20, 95 percent CI: 1.01, 1.43)and women (RR 1.26, 95 percent CI: 1.12, 1.43) also hadincreased mortality.

Excluding the first 5 years of follow-up changed the shapeof the association, particularly in the underweight cate-

gory. While underweight men no longer had a significantincrease in mortality (RR 1.17, 95 percent CI: 0.84, 1.63),underweight women still had the highest mortality, although

TABLE 2. Relative risk of all-cause mortality by body mass index* (BMI) category at study entry, Leisure World Cohort Study,

19812004

BMI categoryMedian

BMIBMI

rangeNo. of

participantsNo. ofdeaths

Model 1y Model 2z Model 3

RR{ 95% CI{ RR 95% CI RR 95% CI

All participants

Underweight (BMI


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TABLE 4. Relative risk of all-cause mortality by category of weight change from age 21 years to study entry, Leisure World Cohort S

Weight change categoryWeight change (%) Weight change(pounds*) No. of

participantsNo. ofdeaths

Model 1y

Median Range Median Range RR{ 95% CI{

Underweight (BMI{,# 5% 10 32.7 to 5.1 10 34 to 5 37 34 1.93 1.37, 2.70 1

Stable weight (within 5%) 0 5.0 to 5.0 0 6 to 6 147 137 1.48 1.24, 1.76 1

Weight gain 5.115% 10.6 5.1 to 15.0 11 5 to 20 260 215 1.12 0.97, 1.28 1

Weight gain >15% 30 15.1 to 104.5 31 13 to 100 964 768 0.97 0.90, 1.06 0

Normal weight (BMI 18.524.9)at age 21 years

Weight loss >5% 9.6 33.3 to 5.0 13 55 to 5 1,293 1,169 1.28 1.19, 1.37 1

Stable weight (within 5%) 0.8 5.0 to 5.0 1 9 to 10 2,725 2,275 1.00 Reference 1

Weight gain 5.115% 9.7 5.0 to 15.0 12 5 to 25 3,324 2,728 0.96 0.91, 1.01 0

Weight gain >15% 23 15.0 to 141.4 30 15 to 164 3,672 2,966 0.97 0.92, 1.02 0

Overweight/obese (BMI 25)at age 21 years

Weight loss >5% 12.5 53.6 to 5.1 20 133 to 7 441 403 1.26 1.13, 1.40 1

Stable weight (within 5%) 0 5.0 to 5.0 0 10 to 10 273 241 1.05 0.92, 1.20 1

Weight gain 5.115% 8.8 5.1 to 15.0 15 7 to 30 201 173 1.09 0.93, 1.27 1

Weight gain >15% 19.8 15.2 to 84.4 30.5 20 to 135 114 94 1.32 1.08, 1.63 1

* 1 pound 0.45 kg.

y Results were adjusted for age at entry, gender, and smoking.

z Results were adjusted for age at entry, gender, smoking, and active activities (seven categories).

Results were adjusted for age at entry, gender, smoking, active activities (seven categories), and history of hypertension, angina, myoca

and cancer.{ RR, relative risk; CI, confidence interval; BMI, body mass index.

# Weight (kg)/height (m)2.

AmJEpidemiol2

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the relation was somewhat attenuated (RR 1.41, 95 per-cent CI: 1.26, 1.59).

DISCUSSION

Our 23-year follow-up study suggests that all-cause mor-tality in older adults is increased among persons who are

underweight or obese during old age and among personswho were overweight or obese at age 21 years. Both weightloss between age 21 and later life (regardless of weight atage 21) and being underweight at age 21 but not gainingweight later in life were associated with increased mortality.Conversely, being of normal weight at age 21 and gainingweight by late adulthood was associated with decreasedall-cause mortality.

FIGURE 1. Relative risk of all-cause mortality according to body mass index (BMI; weight (kg)/height (m)2

) category at study entry for never, past,and current smokers, Leisure World Cohort Study, 19812004. Results were adjusted for gender and age at entry. The normal weight categorywithin each smoking group was used as the reference category. Bars, 95% confidence interval.

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To maintain the population-based characteristic of oursample, we included in our analyses some participants whowere younger than age 65 years at entry. Although, by ourdoing this, some participants did not fall into the elderlycategory, 97 percent of the person-years in our study werefor persons aged 65 years or older. In addition, results for

analyses excluding persons under age 65 years at entry (notshown) were essentially unchanged.

The shape of the association between BMI and mortalityin the elderly remains controversial (1, 12). Most studieshave found the association to be U-shaped (1322) orJ-shaped (15, 16, 20, 21, 23, 24) in all or a subset of the

FIGURE 2. Relative risk of all-cause mortality according to body mass index (BMI; weight (kg)/height (m)2) category at study entry fordifferent agegroups at entry, Leisure World Cohort Study, 19812004. Results were adjusted for gender and smoking status. The normal weight category withineach age group was used as the reference category. Bars, 95% confidence interval.


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subjects under study. However, other studies have founda positive linear association (7, 13, 25), a negative linearassociation (2630), or no association (25, 27, 3134).

The variations in the shape of the association betweenBMI and all-cause mortality among studies may be due todifferences in the age composition of the cohorts, the lengthof follow-up, and the variables that were adjusted for in the

analyses, as well as inclusion or exclusion of smokers orearly deaths. Two studies with long follow-up in the elderlyhave found a reverse J-shaped association (2, 23). The re-sults of these studies agree with our finding that persons inthe lowest weight category, regardless of age, adjustment forother confounders, or exclusion of early deaths, have thehighest mortality.

The reason for increased mortality among the under-weight elderly is not clear. Being lean may represent a realrisk because of nutrient deficiency, frailness, and reducedfunctional status (23). Persons with underlying disease andincreased mortality are more likely to be underweight. Inour study, however, the highest mortality was observed

among the underweight even after exclusion of the first5 years of follow-up. In some studies, increased mortalitywith low BMI has been seen only among smokers or thevery old (15, 23). We observed increased mortality in theunderweight regardless of smoking status or age. Persons inthe underweight category in this study may represent a mixof those who chose to be lean and those who were under-weight because of illness (35). It may also be a mix, espe-cially in the elderly, of persons with low muscle mass andpersons with low fat mass (30). Adjustments for recentweight changes and other measures of assessing body com-position are important in order to pinpoint the reasons forincreased mortality among the underweight elderly. None-

theless, our results are fairly robust in showing that under-weight elderly have higher mortality than normal-weightelderly.

While the authors of a recent meta-analysis of the asso-ciation between adiposity and all-cause mortality empha-sized the importance of adjusting for physical activity (5),the summary relative risk for an elevated BMI from thestudies that included physical activity as a covariate (RR 1.23) was almost identical to the risk from the studies thatdid not (RR 1.24). Consistent with this finding, our resultswere similar regardless of whether or not we adjusted forphysical activities.

It has been suggested that adjusting for factors such ashypertension and diabetes in regression analyses represents

overadjustment and produces biased estimates (6, 7), sincethese factors are biologic intermediates on the causal path-way between obesity and mortality rather than confounders.Adjustment for the specified medical conditions changedour results little.

The strategy of excluding early follow-up has been usedin many studies to account for the potential effect of un-derlying disease. Some simulation studies have indicatedthat exclusion of the first few years of follow-up is not aneffective way of dealing with confounding due to occultdisease and that it may, in some circumstances, exacerbatethis confounding (3638). However, investigators fromanother simulation study concluded that under certain as-

sumptions this method could be very effective (39). None-theless, although our results showed some changes in themagnitude of the relative risk estimates with exclusion ofthe first 5 years of follow-up, the main conclusions wereunchanged.

The influence of age on the relation between BMI andmortality has not been widely studied, especially in the el-

derly. The few available studies suggest that the associationbetween increased weight and higher mortality is primarilyrelevant for the younger elderly. A study with over 12 yearsof follow-up (23) found that greater BMI was associatedwith higher mortality only up to 75 years of age. Beyondage 75, increased BMI was associated with increased mor-tality only among men, and above age 85, low BMI wasassociated with higher mortality only among women. An-other study with 14 years of follow-up found an associationbetween high BMI and increased mortality at all ages, whilelow BMI was associated with mortality only among personsaged 75 years or more (15). In contrast, for all age groups inour study, the highest mortality was among underweight

participants. Obese participants had increased mortalityonly among persons aged less than 75 years.

Many studies deal with the effect of smoking on the BMI-mortality relation by including it as a covariate in the anal-yses, while other studies analyze only nonsmokers. Theauthors of one report concluded that the association betweenBMI and all-cause mortality is present in both smokers andnonsmokers but the effects of underweight, overweight, andobesity may differ depending on smoking status (5). An-other study found a positive linear association betweenBMI and mortality among never smokers but no associationamong recent former smokers or current smokers (35). Wefound increased mortality among the underweight regard-

less of smoking status, while mortality was increased inobese never and past smokers but not in current smokers.It is possible that the harmful effect of obesity is overshad-owed by the harmful effect of smoking, so that obese smok-ers do not show higher mortality when compared withnormal-weight smokers.

Although some studies have found differences in theBMI-mortality association for men and women (20, 27),our risk estimates for men and women were almost identi-cal. The only difference was found when early follow-upwas excluded, resulting in greater attenuation of the relativerisk for underweight men than for underweight women.

Few studies have reported on the effects of being over-weight or obese in early adulthood on all-cause mortality in

later life. The available findings are consistent with our re-sults showing increased mortality in the overweight or obese(29, 40, 41). Since our cohort was 73 years of age at entry,on average, most were aged 21 years during the 1920s and1930s. The prevalence of overweight and obesity has greatlyincreased since then, especially in the past few decades (42).Even though the proportion of persons who were obese atage 21 in our study was smaller than the proportion of obese21-year-olds today, we have no reason to believe that theobserved associations should not apply to those who areaged 21 now. However, since our study included only peoplewho survived to enter the retirement community, the effectof weight at age 21 on mortality in our study is limited to its

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effect in old age and does not reflect its effect on mortalitybetween age 21 and age at entry.

While many studies of the association between weightchange and all-cause mortality have been conducted, theresults are difficult to compare among studies because ofdifferences in the time period between the two weight mea-sures, the length of follow-up, and how weight change is

expressed. Increased mortality has been associated withweight loss in most studies of weight change (19, 26, 27,4350), but in other studies it has been associated withweight gain (24, 51, 52), both weight loss and extremeweight gain (35, 5358), or neither (59, 60). In contrast toour findings, the few studies most similar to ours in terms ofweight change over a long time period and follow-up peri-ods of more than 20 years have mostly shown increasedmortality with weight gain (24, 51, 52). The differencesbetween those results and ours might be explained by theolder age of our participants.

The benefit of gaining weight throughout life was re-ported in 1985 with the publication of tables of ideal weight

(61), where the lowest mortality occurred at progressivelyincreasing body weight with advancing age (5 kg per de-cade). Although our most consistent finding was that weightloss was associated with increased mortality, we also sawevidence of benefit with weight gain among persons whowere underweight or of normal weight at age 21. The sta-tistical significance of these findings, however, depended onwhether or not adjustment was made for other confoundersand on whether early follow-up was excluded.

When interpreting our results regarding weight change,it is important to note that we were able to evaluate onlyweight change between age 21 years and the age at whichthe questionnaire was completed (an average period of 52

years). We were unable to determine when the weightchange occurred or to distinguish between gradual weightchange and rapid weight change, fluctuating weight andrelatively stable weight, and intentional weight change andunintentional weight change. All of these factors may beimportant in analysis of the effect of weight change onmortality (12, 44, 62).

Other limitations included the use of self-reported dataon height and weight and recall of weight at age 21 years.The validity and reliability of such data are controversial.Although we previously found relatively good agreement(>90 percent) in this population between self-reportedheight and weight and height and weight obtained from med-ical records (8), some studies suggest that bias in reporting of

height and weight varies with weight, such that overweightand obese persons are more likely to underreport their weightthan normal- or underweight persons (63, 64). This under-reporting would result in misclassification of participantswhen using standard weight categories. A strategy for deal-ing with this potential misclassification is to analyze rankeddata such as quintiles. Although we did not report thoseresults, we obtained very similar findings when the data wereanalyzed in quintiles: increased mortality among persons inthe lowest and highest quintiles of BMI, with the highestmortality being seen among persons in the lowest quintile.

Despite its limitations, our large, population-based, long-term study of older adults with almost complete follow-up

provides important information on the relations of weightand weight change to mortality in the elderly. We were ableto adjust for several important confounding variables and toexplore the modifying effects of smoking status, age, andgender. Our study highlights the risks on mortality in olderage of being overweight or obese in young adulthood andunderweight or obese in later life.

ACKNOWLEDGMENTS

This research was funded by grants from the NationalInstitutes of Health (R01CA32197 and R01AG21055), theEarl Carroll Trust Fund, and the Al and Trish Nichols Chairin Clinical Neuroscience.

Conflict of interest: none declared.

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Documents

Association of BMI and Weight Change With All Cause Mortality in Elderly