© 1998 American Heart Association, Inc.
Original Contributions |
Serial Changes in Body Composition Throughout Adulthood and Their Relationships to Changes in Lipid and Lipoprotein Levels
The Fels Longitudinal Study
From the Division of Human Biology, Department of Community Health, Wright State University School of Medicine, Yellow Springs, Ohio.
Correspondence to Dr R.M. Siervogel, Division of Human Biology, Department of Community Health, Wright State University School of Medicine, 1005 Xenia Ave, Yellow Springs, OH 45387-1695. E-mail rsiervog{at}discover.wright.edu
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Abstract |
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Abstract—Few studies have examined the relationships between measures of body composition and lipid and lipoprotein levels in long-term serial data from individuals unselected for cardiovascular disease– or obesity-related variables, and none have considered such extensive serial data as used in the current study. The aim was to examine in such individuals the associations between annual changes in lipid and lipoprotein levels and concurrent changes in total body fat, fat-free mass, percent body fat, and body mass index. Serial data from 1304 examinations of 423 adult white participants in the Fels Longitudinal Study were analyzed sex-specifically in 2 age groups, 18 through 44 years and 45 to 65 years. A regressive analytic approach utilized the long-term (4 to 20 years) serial data of individuals. Annual changes in adiposity, independent of levels of lean tissue changes, before and after age 45 for men and women were significantly correlated with corresponding annual changes in cholesterol and low density lipoprotein cholesterol. In men before age 45, changes in triglycerides and high density lipoprotein cholesterol were also significantly associated with changes in adiposity, with the relationship remaining after age 45 in high density lipoprotein cholesterol. Increases in adiposity in individuals are associated with changes in lipid and lipoprotein levels in the direction of increased risk for cardiovascular disease. Adult levels of total cholesterol and low density lipoprotein cholesterol across age and sex and high density lipoprotein cholesterol in men are responsive to changes in adiposity, independent of initial adiposity or lipid and lipoprotein levels.
Key Words: body composition • fat-free mass • lipids • lipoproteins • serial
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Introduction |
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Cross-sectional population studies in the United States have clearly demonstrated age-associated increases in serum lipid and lipoprotein levels, body weight, and indices of body fatness in adults.1 2 In addition to adiposity, elevated levels of total (TC) and LDL cholesterol (LDL-C) are risk factors for coronary heart disease, as is a reduced level of HDL cholesterol (HDL-C).3 4 5 In both obese and nonobese individuals, weight loss over short periods of time is commonly associated with a decrease in TC levels.6 7 8 Cross-sectional relationships between lipids and lipoproteins and body composition in young, middle-aged, and older adults have shown that adiposity and adipose tissue distribution are related to lipid and lipoprotein levels.9 10 11 12 13 In addition, a few follow-up studies have shown relationships between changes in adiposity and changes in lipids and lipoproteins over some age ranges.14 15 16 However, in the United States, there is relatively little information about the relationships between changes in body composition throughout adulthood and concurrent changes in lipid and lipoprotein levels in individuals unselected for variables related to cardiovascular disease or obesity. The aim of the current study was to examine in such individuals the associations between average annual changes in plasma lipid and lipoprotein levels and concurrent changes in total body fat, fat-free mass (FFM), percent body fat (%BF), and body mass index (BMI).
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Methods |
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Data recorded since 1976 from 1304 examinations of a subset of 423 white adults (202 men, 221 women) enrolled in the Fels Longitudinal Study17 were analyzed. Participants in this study have been enrolled between 1929 to the present, typically near the time of their birth. Most are white, were residing in southwestern Ohio at the time of their enrollment, and were selected for enrollment on the basis of the willingness of their parents to allow them to participate in a long-term serial study. The National Center for Health Statistics' United States growth charts for children from birth to 36 months are based exclusively on data from participants in the Fels Longitudinal Study.18 Adult participants between the ages of 25 and 40 are scheduled for examinations every 5 years, and those residing out of state are also scheduled at 5-year intervals regardless of age. All other adults are examined every 2 years.
Body density was determined by hydrodensitometry.19 Body composition measures of total body fat (TBF, kg), %BF, and FFM (kg) were calculated by using Lohman's multicomponent model over a wide age range.20 This approach allows for age and sex variation in the composition of FFM up to age 25 years and, in a comparison of several body composition methodologies in this population, it performed well across the adult age range considered here.21 BMI (kg/m2) was calculated from weight and stature. Plasma levels of fasting TC (mmol/L), HDL-C (mmol/L), LDL-C (mmol/L), and triglycerides (TG, mmol/L) were measured according to standard procedures.22 23 24 All data collection procedures were approved by the Institutional Review Board of Wright State University, and the participants in this study gave their informed consent to be involved in the research.
Two age groups were analyzed separately, 1 including
participants between 18 and 44 years of age and 1 with participants
ranging from 45 to 65 years of age. For inclusion within an age group,
participants had to have at least 2 examinations within the specified
age range, with the first and last examination separated by an interval
of at least 4 years. For each individual, interval length was
calculated as the difference in years between the first and last
examinations within an age range, and median age (midage) was
calculated as the mean of the ages at the first and last examinations.
For each individual with >2 examinations, a series of linear
regressions, with age as the independent variable and with each
body composition or lipid and lipoprotein measure as the dependent
variable, was used to determine an annualized rate of change, or
slope, for each variable. For individuals with exactly 2
examinations within an age group, the difference between last and first
examinations divided by interval length was used as a measure of
annualized change in each lipid or lipoprotein and body composition
variable. The regressive approach maximizes the information in each
person's serial data and should provide better estimates of the rate
of change than simply using the end points, as is typically done in
studies with a "follow-up" design. The resulting variables for
changes were 
TBF (kg/y), %BF (%/y), FFM (kg/y), BMI
(kg · m-2 ·
y-1), TC (mmol ·
L-1 · y-1),
HDL-C (mmol · L-1 ·
y-1), LDL-C (mmol ·
L-1 · y-1), and
TG (mmol · L-1 ·
y-1).
t Tests were performed to determine sex differences and
whether or not annualized rates of change were different from zero.
Significant differences were defined at the P<0.05 and
P<0.001 levels. To account for individual baseline levels,
a regression of baseline level for each body composition and lipid and
lipoprotein variable on their corresponding annual change was
performed within each age and sex group. The corresponding
baseline-adjusted variables are identified by a preceding
a (eg, aTBF and
aTC). The associations between the
baseline-adjusted annual rate of change in each body composition
measure and the baseline-adjusted annual rate of change in each lipid
and lipoprotein measure were described by using Pearson's
product-moment correlations calculated separately for men and women
in each age group. To adjust FFM for level of adiposity, a linear
regression of TBF on FFM was first performed within each age group, and
the individual regressive analytic approach described above was then
applied to the residuals.
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Results |
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The number of individuals with each of the various numbers of serial examinations within each age group is given in Table 1
. The number of serial examinations for
the younger age group ranges from 2 to 6, with 
65% of the
individuals in this age group having 3 or more examinations. In the
older group, the number of examinations ranges from 2 to 7, with 75%
having 3 or more examinations and 18% of the individuals having 5 or
more examinations.
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The means for the midage, interval, body composition measures, and
lipid and lipoprotein levels are given in Table 2. The means of the body composition and
lipid and lipoprotein variables within each age group were based on
the individual regressions and calculated at the midage. The mean age
in each of the 2 age groups was approximately 30 and 54 years,
respectively, for both men and women, and the mean age interval was
between 9.4 and 11.2 years for each agexsex group. The sex differences
observed in the younger age group were consistent with
expectations based on the published literature; women had higher levels
of TBF, %BF, and HDL-C and men had higher levels of FFM, TC, LDL-C,
and TG. BMI values were similar for both sexes. The differences between
the means for adiposity and lipid and lipoprotein variables between
younger and older men and women were consistent with an
increasing risk in each cardiovascular disease risk
factor studied, except there were no changes in mean HDL-C for men, and
there were only slight increases in mean HDL-C levels for women. FFM
(uncorrected for TBF) was not different between younger and older men
or women.
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The means and SDs for the annual change variables for each
agexsex group are given in Table 3. For
younger men, all the annual changes in body composition and lipid and
lipoprotein levels (except for HDL-C) were positive and
significantly different from zero. For younger women, BMI, TBF,
%BF, and TG were likewise positive and significantly different
from zero. Significant sex differences in annual changes in the younger
group were found in TC, TG, and LDL-C, with men exhibiting a
greater change in each. The means for BMI, TBF, and %BF in
older men and women were positive and significantly different from
zero. Also, TC and LDL-C in older men were negative, TG in
older women was positive, and all were significantly different from
zero. A significant sex difference in the older group was found in
TC and LDL-C, with men exhibiting a decrease in each.
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The correlations between the baseline-adjusted annual changes in body
composition measures and those of lipid and lipoprotein levels are
presented in Table 4. In the
younger men, each of the baseline-adjusted annual changes in lipids and
lipoproteins was significantly associated with the corresponding
changes in each adiposity measure, aTBF,
a%BF, and aBMI, with
the absolute value of the correlations ranging from 0.23 to 0.49. Also
in the younger men, aFFM (uncorrected for TBF)
was significantly correlated (0.23) with aTG.
In the older men, only baseline-adjusted adiposity measures were
significantly correlated with any of the baseline-adjusted annual
changes in lipids and lipoproteins. The adiposity measures of
aTBF and aBMI were
positively associated with aTC and
aLDL-C, with values ranging from 0.28 to 0.39.
These were not significantly correlated with
aTG, however. All adiposity measures,
including a%BF, were significantly negatively
correlated with aHDL-C. Thus, the pattern of
the relationships between changes in adiposity and changes in lipid and
lipoprotein levels was similar in the older and younger groups of men,
except that aTG was not significantly
associated with any of the adiposity variables in older men.
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For younger women, each of the adiposity measures was significantly
correlated with aTC and
aLDL-C, with magnitudes ranging from 0.20 to
0.32. In addition, aHDL-C was significantly
correlated with both aBMI and
aTBF; aTG was
significantly associated with aBMI. In the
older women, aTC and
aLDL-C were significantly correlated with each
measure of adiposity, with aLDL-C exhibiting a
stronger relationship. The pattern of the relationships between
baseline-adjusted changes in body composition and changes in lipid and
lipoprotein levels was similar in the older and younger groups of
women.
The relationship between changes in FFM, independent of levels of
adiposity, and changes in lipid and lipoproteins in individuals was
also investigated. Because levels of lean tissue increase as the level
of adiposity increases, FFM was adjusted for levels of TBF within each
age range. None of the correlations between the changes in this
TBF-adjusted level of FFM and changes in lipid or lipoprotein levels in
either sex or age group were significant (most correlations were
-0.10
P0.10). Thus, the association between the
changes in lipids and lipoproteins was significantly associated with
the changes in adiposity and not with changes in FFM.
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Discussion |
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The age groupings used in the current study were determined in part from comparison of lipid and lipoprotein data from the Fels Longitudinal Study with cross-sectional data from the second US National Health and Nutrition Examination Survey (NHANES II). As shown in the Figure
, NHANES II data for white
adults show approximately linear increases in mean TC, LDL-C, and TG
levels until approximately 45 years of age, after which there seems to
be a sex-specific difference in the pattern of lipid and lipoprotein
levels across age.2 The mean levels of HDL-C
remain relatively constant from 20 to 74 years. For the purpose of
comparison with NHANES II data, the Fels Longitudinal Study data were
separated into age groups 18 to 24, 25 to 34, 35 to 44, 45 to 54, and
55 to 64 years. These age groups matched those used in describing the
NHANES II distributions, except that the youngest NHANES group was 20
to 24 years of age. Mean lipid and lipoprotein levels within these age
groups were calculated with all available data from the sample
described in the current investigation. Although mean levels of plasma
lipids and lipoproteins of the Fels participants were slightly lower
than the national averages, data from the Fels Longitudinal Study show
a pattern across age similar to that of the NHANES II data, with
approximately linear increases until age 45 years and sex-specific
differences in patterns of change across age after 45 years. Because
the analytic methods used in the current study assume linear changes
across age, the age ranges of 18 to 44 years and 45 to 65 years were
selected to best correspond to periods of approximately linear
cross-sectional change with age. In addition to comparison with
national data,2 25 the assumption of linearity in
each of the age ranges and the dichotomization of age groups at 45
years were also based on scatterplots of the Fels Longitudinal Study
body composition and cardiovascular disease risk factor
data against age.
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The current study is atypical, in that all available serial data within the specific age ranges of each age group were utilized in the analyses. Previous studies investigating changes in lipids and changes in body composition have used a follow-up approach, wherein the differences between measurements taken at 2 points in time were used as measures of change, eg, the Québec Family Study16 and a study using data from western Samoans.26 Although rates of change can be calculated from the values obtained at the first and last examinations for individuals, all intermediate data for each individual are ignored in this approach. In the current study, 65% of the younger group and 75% of the older group had at least 3 measurements, and the intermediate data points comprised 35% of the 1304 total examinations of 423 individuals. Also, the individual regressive approach used in these analyses assumes a linear trend within each age group and therefore minimizes the effects of aberrant values due to measurement error or short-term biological variation.
Differences in the number of measurements for each individual were
primarily a function of the study design rather than loss due to
participant dropout. Adult participants of the Fels Longitudinal Study
are scheduled for examinations at 2- or 5-year intervals depending on
age and geographic location. Also, because the study has added new
participants at a relatively constant rate over the years, some of the
younger participants may have fewer examinations than older
participants, or in fact, may have more examinations than slightly
older participants owing to the study design. The age distribution of
participants when hydrodensitometry was implemented into the Fels
Longitudinal Study in 1976 also accounts for some variation in the
number of examinations. The length of follow-up was affected somewhat
by the number of examinations. Participants with only 2 measurements
had a significantly shorter interval length than did those with >2
examinations, 8 years compared with 11 years for younger males and
females and 7 years compared with 11 years in older males and
females. In addition, the midage of younger females having 2
examinations (31.8 years) was significantly older than that of those
with >2 examinations (29.4 years). None of the other change
variables in either the younger or the older groups were
significantly different with regard to number of examinations.
In the current investigation, correlation coefficients between baseline-adjusted changes in BMI and changes in TC, LDL-C, TG, and HDL-C were examined. The baseline adjustment made for each of the change variables allows for associations to be determined independent of initial adiposity, leanness, or general atherogenic profile. These correlations ranged from -0.33 to 0.49 and were generally greater in younger men than in younger women and similar between the sexes in the older group, suggesting that lipid and lipoprotein levels in young to middle-aged men were more susceptible to biological changes affecting BMI.
Although BMI is often used as an indirect index of adiposity, the body
compartments of TBF and FFM are often confounded in associations
between BMI and lipids and lipoproteins. The current study indicates
that the correlations between both aBMI and
aTC and aBMI and
aLDL-C reflect a relationship between the
specific cholesterol variable and
aTBF for younger and older men and women. Only
in younger men was the FFM compartment of BMI associated with changes
in lipid or lipoprotein levels; aFFM was
significantly correlated with aTG. The other
adiposity measure, a%BF, was significantly
correlated with aTC and
aLDL-C in the younger men and in both younger
and older women. In addition, aHDL-C was
significantly related, albeit negatively, to all of the adiposity
measures in the younger and older men. Not addressed in this study is
which relationships, if any, may exist between changes in adipose
tissue distribution independent of overall adiposity and changes in
lipid and lipoprotein levels in individuals. Although some
investigators have reported independent effects of abdominal obesity on
lipid and lipoprotein levels after adjustment for BMI or other measures
of adiposity,27 28 Jakicic and
associates29 concluded that obesity was necessary
for the relationships between various anthropometric measures of fat
distribution and lipids and lipoproteins to exist. Likewise, Couillard
and colleagues16 reported that 12-year changes in
the distribution of subcutaneous fat were not independently correlated
with lipid and lipoprotein profiles after controlling for variation in
TBF.
The average interval of 10 years within each age and sex group
in the Fels Longitudinal Study sample was long enough for significant
changes in the measured variables to occur. In men, the rate of
increase in adiposity was more pronounced before age 45 compared with
those observed at older ages, whereas in women, the rate of increase
was similar both before and after age 45. In men, mean rates of change
in TC levels increased to middle age, after which a decreased rate of
change was noted. In women, the rate of increase was considerably
slower and continued after age 45 years. Because the individuals
enrolled for these analyses were unselected with regard to
disease and generally represent a "normal" sample, the
strong, positive correlations between the baseline-adjusted annual
change in adiposity and change in cholesterol levels
suggest that cholesterol levels appear to change with
corresponding changes in adiposity over the whole range of body
composition variation and not just in overweight individuals.
The current findings were compared with those of the Québec
Family Study,16 which examined concurrent
relationships between changes in body fatness and changes in lipid and
lipoprotein levels over a similar time interval (12 years) as that used
in this investigation. Whereas the investigators of the Québec
Family Study concluded that a significant association existed between
changes in fat indices and changes in TC in women, they did not find
significant associations in men. Although this result may be a function
of the considerably smaller sample sizes used in the Québec
Family Study,16 it is more likely to be a
function of the age range studied. The mean ages at baseline and
follow-up for men were 43 and 55 years, respectively, and 41 and 53
years for women, and thus, bridge the break point at 45 years of age
used in the current analysis. As seen in the Figure
and other
sources, the rates of change in lipids and lipoproteins before and
after age 45 years differ.2 11 25 30 31 In the
Québec Family Study, the mean change in TC levels over the entire
12-year follow-up period for men was 0.02 mmol/L. Because the
current study found that TC levels increased before age 45 years at a
rate similar to the rate of decrease after this age, this result is not
surprising, and the lack of association between changes in TC and
changes in body composition in men could be attributed to this
fact.
Other follow-up studies of similar duration have used indirect
measures of adiposity rather than hydrostatic weighing to determine the
effects of changes in body composition on changes in lipid profiles in
both young and old adults. In a study of young Samoan men with a mean
baseline age of 26 years, 10-year changes in abdominal adiposity were
positively associated with changes in TC and non-HDL–C, with
correlations near 0.38.26 These correlations were
similar to those reported in the current investigation for the
baseline-adjusted changes in the direct measures of adiposity with
baseline-adjusted changes in TC and LDL-C. In a study of elderly Dutch
men >58 years of age, Weijenberg and
associates31 reported a decrease in levels of TC
of 0.04 mmol · L-1 ·
y-1, as well as relatively stable levels of
HDL-C over a 15-year follow-up period. This Dutch sample had a mean
midage of 70 years31 and was thus considerably
older than the present 45- to 65-year age group. However, the
findings of Weijenberg and associates31 are
concordant with the serial decreases in TC of older men that were
observed in the current study, as well as with the cross-sectional
decreases observed in TC levels in men as reported by
others,2 25 30 and suggest that these decreases
continue into the eighth decade of life.
Existing parallels were noted between the findings of the current investigation and those designed to examine the effects of weight loss. Intervention studies have shown that weight loss for obese individuals over short periods of time results in an improved atherogenic profile.6 7 8 The lengths of these studies were short, though (<2 years), and the samples were not representative of the general population. However, in a normal Australian sample,15 2-year changes in weight showed relationships generally similar to those observed in the younger adults of the current study; ie, weight changes were significantly associated with changes in all lipid and lipoprotein variables in men and were significantly associated with changes in TC, LDL-C, and TG in women.
The current study has provided strong evidence that there is a positive relationship between changes in TC and LDL-C and concurrent changes in measures of adiposity in young to middle-aged and middle-aged to older groups of white men and women. In addition, young to middle-aged men showed a strong relationship with HDL-C and TG, with this strong relationship in HDL-C continuing into older age. The annual rate of change in adiposity over an average 10-year interval can explain from 4% to 25% of the variation in the annual rate of change in specific lipid or lipoprotein levels. This is somewhat remarkable, considering that these relationships exist irrespective of consideration of the underlying mechanisms (eg, diet, physical activity, etc) that may be involved in specific changes in individuals. Nevertheless, the findings clearly demonstrate that consistent increases in adiposity in individuals are associated with changes in lipid and lipoprotein levels in the direction of increased risk for cardiovascular disease. Adult levels of TC and LDL-C across age and sex and of HDL-C in men are responsive to changes in adiposity, independent of initial adiposity or lipid and lipoprotein levels.
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Acknowledgments |
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This work was supported by grants R01-HD12252 (to R.M.S.) and R01-HD27063 (to S.S.G.) from the National Institute of Child Health and Human Development.
Received December 23, 1997; accepted May 4, 1998.
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