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American Journal of Clinical Nutrition, Vol. 80, No. 3, 576-583, September 2004
© 2004 American Society for Clinical Nutrition

ORIGINAL RESEARCH COMMUNICATION

Serum leptin concentrations and body adipose measures in older black and white adults1,2,3

Constance E Ruhl, James E Everhart, Jingzhong Ding, Bret H Goodpaster, Alka M Kanaya, Eleanor M Simonsick, Frances A Tylavsky and Tamara B Harris for the Health, Aging, and Body Composition Study

1 From Social and Scientific Systems, Inc, Silver Spring, MD (CER); the National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Department of Health and Human Services, Bethesda, MD (JEE); the Laboratory of Epidemiology, Demography, and Biometry, National Institute on Aging, National Institutes of Health, Department of Health and Human Services, Bethesda, MD (JD and TBH); the Division of Endocrinology and Metabolism, University of Pittsburgh, Department of Medicine, Montefiore Hospital, Pittsburgh, PA (BHG); the Department of Medicine, University of California, San Francisco (AMK); the Intramural Research Program, National Institute on Aging, Baltimore, MD (EMS); and the Department of Preventive Medicine, University of Tennessee, Memphis (FAT)

2 The Health, Aging, and Body Composition Study was funded by the National Institute on Aging (contract numbers N01-AG-6-2106, N01-AG-6-2101, and N01-AG-6-2103). The current work was supported by a contract from the National Institute of Diabetes and Digestive and Kidney Diseases (N01-DK-1-2478).

3 Address reprint requests to CE Ruhl, Social and Scientific Systems, Inc, 8757 Georgia Avenue, 12th floor, Silver Spring, MD 20910. E-mail: cruhl{at}s-3.com.


   ABSTRACT
TOP
 ABSTRACT
INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Background: Among US adults, serum leptin concentrations are higher in women than in men and are higher in blacks than in whites independent of anthropometric measures of body fatness.

Objective: Using radiographic measures of body fat, we determined the best correlates of leptin and whether adiposity can explain sex and race differences in leptin concentrations in older adults.

Design: This was a cross-sectional analysis of fasting serum leptin concentrations and body fat measured by dual-energy X-ray absorptiometry (DXA), abdominal computed tomography, and standard anthropometry in 3026 well-functioning 70-79-y-old participants (42% black, 51% women) of the Health, Aging, and Body Composition Study.

Results: Geometric mean (±SE) leptin concentrations (ng/mL) were higher in the women than in the men (16.5 ± 0.3 and 5.7 ± 0.1, respectively) and in the black women than in the white women (20.2 ± 0.6 and 13.9 ± 0.4, respectively), but did not differ significantly between the white and black men (5.8 ± 0.2 and 5.5 ± 0.2, respectively). Percentage fat estimated from DXA showed the highest correlation with leptin (R2 = 0.56 for both sexes). Addition of abdominal visceral fat minimally increased the correlation. In the multivariate analysis, the association with sex was eliminated after adjustment for percentage fat and visceral fat in both whites (P = 0.051) and blacks (P = 0.34). Among women, higher leptin concentrations in blacks remained after adjustment for percentage fat and visceral fat (mean race difference = 4.95 ng/mL; P < 0.001). Among men, an association with black race emerged after adjustment for these factors (mean race difference = 1.42 ng/mL; P < 0.001).

Conclusions: Among older adults, higher serum leptin concentrations in women are explained by a greater percentage of body fat. Higher leptin concentrations in blacks are not explained by percentage of body fat.

Key Words: Leptin • body composition • anthropometry • dual-energy X-ray absorptiometry • computed tomography • race • epidemiology • Health • Aging • and Body Composition Study • Health ABC Study


   INTRODUCTION
TOP
 ABSTRACT
 INTRODUCTION
SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 
Leptin, the protein product of the ob/ob gene, was initially identified as an adipocyte-derived hormone involved in the regulation of energy intake and expenditure (1). Serum leptin concentrations reflect the amount of energy stored in adipose tissue, although most obese humans have a resistance to leptin (2). Leptin is also synthesized in other tissues and has many additional functions, including the regulation of glucose homeostasis, blood vessel growth, and the reproductive and immune systems (3).

Several studies have consistently found women to have higher serum leptin concentrations than do men (4-10). For example, among US adults across a broad age range, the mean serum leptin concentration was much higher in women (12.7 µg/L) than in men (4.6 µg/L) (4). Although sex differences in leptin concentrations are believed to stem from differences in body composition, particularly body fatness, estimates based on anthropometry do not completely explain the sex differences. We hypothesized that more precise assessment of body composition would further attenuate or totally eliminate the sex differences in serum leptin.

Few studies have investigated whether serum leptin concentrations differ by race/ethnicity. Among US adults across a broad age range, mean serum leptin was slightly but significantly higher in non-Hispanic blacks than in non-Hispanic whites of both sexes after adjustment for skinfold thicknesses and circumferences (4). It is unclear whether this difference was the result of imprecise adjustment for adiposity. The relation between leptin concentrations and race/ethnicity has been examined in few other population-based studies, most of which have not found major ethnic differences (9, 11). More precise measures of body fat would be useful in determining whether racial differences in serum leptin exist.

In a large, biracial cohort of older adults, we determined the best predictors of leptin by using anthropometric and body fat measures. These measures were then used to investigate whether sex and race differences in leptin concentrations could be explained by adiposity among older adults.


   SUBJECTS AND METHODS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
RESULTS
 DISCUSSION
 REFERENCES
 
The Health, Aging, and Body Composition Study is a longitudinal study of 3075 community-dwelling, well-functioning white and black men and women aged 70-79 y at study entry. The study was designed to investigate changes in body composition, weight-related health conditions, and incident functional limitations (12). Participants were recruited from a random sample of white Medicare beneficiaries and all age-eligible black community residents residing in designated ZIP codes in the metropolitan areas surrounding Pittsburgh and Memphis. The sample was selected to represent well-functioning older persons. Eligibility criteria included no report of any difficulty walking 0.40 km (0.25 mile), walking up 10 steps, or performing basic activities of daily living. In addition, persons who reported active treatment for cancer within the past 3 y, were planning to move out of the area within 3 y, or were actively enrolled in a diet or exercise intervention study were excluded. The study was approved by the Institutional Review Boards at the Universities of Pittsburgh and Tennessee, and all participants provided written informed consent to participate. The present study used cross-sectional data from the baseline examination conducted between 1997 and 1998 and included 3026 participants with data on serum leptin concentration.

Serum leptin concentrations were measured in duplicate by radioimmunoassay in venous blood samples collected in the morning from fasting subjects (Linco Research Inc, St Charles, MO) (13). The minimum concentration detectable with use of this assay is 0.05 ng/mL. Intraassay CVs ranged from 3.7% to 7.5%, and interassay CVs ranged from 3.2% to 8.9%. Fasting serum leptin concentrations ranged from 0 to 54.7 ng/mL. For 155 participants, leptin concentrations were outside of the linear range of the assay and were not on the linear portion of the standard curve. These numerical values were not recorded by the laboratory and were recoded for the present analysis as 52 ng/mL, the upper limit of the curve specified by Linco Research Inc.

Height, weight, abdominal and thigh circumferences, and sagittal diameter were measured. Height was measured to the nearest millimeter by using a Harpenden stadiometer (Holtain Ltd, Crosswell, United Kingdom) with the participant barefoot, and weight was measured to the nearest 0.1 kg by using a standard balance beam scale with the participant wearing lightweight clothing. Abdominal and thigh circumferences were measured to the nearest 0.1 cm: abdominal at the maximum circumference and thigh at the midpoint between the inguinal crease and the proximal border of the patella. Abdominal sagittal diameter was measured by using a Holtain-Kahn abdominal caliper (Holtain Ltd) at the level of the iliac crests with the participant supine with knees bent at a 45 ° angle. BMI [weight (kg)/height (m2)] and abdominal-to-thigh circumference ratio were calculated.

Arm, leg, trunk, and total body fat were estimated from dual-energy X-ray absorptiometry (DXA; QDR 4500A; Hologic Inc, Waltham, MA; software version 8.21 for analysis), and total percentage body fat was calculated. Abdominal subcutaneous and visceral fat areas, thigh subcutaneous and intermuscular fat areas, and thigh muscle density (inversely related to muscle lipid content) were measured by using computed tomography (CT) with a 9800 Advantage (General Electric, Milwaukee) in Pittsburgh or a Somatron Plus 4 (Siemens, Erlangen, Germany) or Picker PQ2000S (Marconi Medical Systems, Cleveland) in Memphis. Ten-millimeter scans were obtained of the abdomen at the L4-L5 level and of the thigh at the midthigh level. Data from the CT scans were analyzed at the University of Colorado Health Sciences Center according to a standardized protocol (14, 15). Thigh length was measured from the CT scout image and thigh length-to-height ratio was calculated.

Statistical analysis
Leptin concentrations were log transformed to normalize the distribution. Means and standard deviations for leptin concentration and body fat measures were calculated, and means were compared between sex and race subgroups by using t tests or Wilcoxon’s nonparametric tests. The relation of leptin concentration with body adipose measures was examined by using multiple linear regression analysis. Analyses were adjusted for age, field center site, and race (in analyses of men and women). Quadratic terms for body fat measures were also considered for inclusion by adding them individually to multivariate models. Interactions were tested for by using analysis of variance (ANOVA) and analysis of covariance (ANCOVA). To investigate whether sex and race differences in leptin concentrations were explained by body fat distribution, sex or race was included in multivariate regression models while adjusting for body adipose measures. P values <0.05 indicated statistical significance. Analyses were performed by using SAS 8.2 software (16).


   RESULTS
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
DISCUSSION
 REFERENCES
 
Serum leptin concentrations and anthropometric and body fat measures were performed on 926 white men, 542 black men, 840 white women, and 718 black women. Serum leptin concentrations were higher in the women than in the men and were higher in the black women than in the white women but did not differ significantly between the white and black men (Table 1Go). Total percentage fat was higher in the women than in the men and, within a sex, was higher in black women and in white men. Of the other body fat measures, all except for abdominal visceral fat were higher in the women. Among the women, body weight and all body adipose measures were higher in blacks than in whites, except for abdominal visceral fat, which did not differ significantly by race/ethnicity. Among the men, whites had greater abdominal visceral fat by CT and greater trunk fat by DXA, whereas blacks had greater thigh subcutaneous and intermuscular fat by CT and greater leg fat by DXA. Tests for sex-race interactions were significant (P < 0.05) for serum leptin and all but 3 of the 19 anthropometric and body adipose measures listed in Table 1Go.


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  		TABLE 1 Characteristics of the study sample by sex and race

 
In age- and site-adjusted analyses, serum leptin concentrations were strongly associated with all measures of body fat (Table 2Go). With the exception of thigh subcutaneous fat, tests for the interaction of sex, race, and each fat-related measure on leptin were significant (P < 0.05). The amount of variance in leptin concentrations explained by body adipose measures did not differ greatly among sex-race subgroups. The DXA estimate of total percentage fat had the strongest correlation with leptin concentration of any measure (R2 = 0.56 for men and women). Adding a quadratic term for total percentage fat increased the R2 in men to 0.60 and that in women to 0.58.


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  		TABLE 2 Age- and site-adjusted associations (R2) of log serum leptin concentration (ng/mL) with anthropometric and body adipose measures1

 
To investigate whether specific fat depots, as measured by CT, accounted for additional variance in leptin concentrations beyond that explained by total percentage fat, we added individual fat depot measures to models containing percentage fat linear and quadratic terms. Very little additional variance in leptin concentrations was explained by adding fat depot measures. Abdominal visceral fat made the greatest added contribution but accounted for only an additional 1-2% (Table 3Go). Adding more than one regional fat measure did little to increase the R2. Percentage fat remained associated with leptin concentrations independent of each of the fat depot measures in both sexes and races (P < 0.001; data not shown).


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  		TABLE 3 Age- and site-adjusted associations (R2) of log serum leptin concentration (ng/mL) with body adipose measures1

 
After determining the relations of leptin concentration with anthropometric and body adipose measures across sex and race subgroups as reported above, we next investigated whether the higher leptin concentrations in the women could be explained by higher percentages of body fat. As expected, before adjustment for body fat measures, higher leptin concentrations were found in both white and black women than in the men (Table 4Go, model 1). However, controlling for percentage fat not only eliminated the higher leptin concentrations in the women, but resulted in the emergence of higher adjusted concentrations in the men (Table 4Go, model 2). Adding abdominal visceral fat to the models eliminated the sex difference in leptin concentrations among both whites and blacks (Table 4Go, model 3). In contrast, BMI differences did not explain the higher leptin concentrations in the women compared with the men. These effects across the range of BMI and percentage fat are shown in Figure 1Go. The sex difference in leptin concentrations was not completely explained by substituting total fat mass for percentage fat.


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  		TABLE 4 Relations of log serum leptin concentration (ng/mL) with sex in whites and blacks

 


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  		FIGURE 1. Geometric mean (±SE) serum leptin concentrations by BMI or total percentage fat decile and sex. BMI cutoffs (kg/m2) for the 1st to 9th deciles, respectively, were as follows: <21.8, 21.8 to <23.4, 23.4 to <24.7, 24.7 to <25.7, 25.7 to <26.9, 26.9 to <28.0, 28.0 to <29.3, 29.3 to <31.0, 31.0 to <33.7, and ≥33.7. Total percentage fat cutoffs for the 1st to 9th deciles, respectively, were as follows: <23.8, 23.8 to <26.6, 26.6 to <28.9, 28.9 to <31.0, 31.0 to <33.6, 33.6 to <36.3, 36.3 to <38.9, 38.9 to <41.6, 41.6 to <44.5, and ≥44.5.

 
Race was evaluated as an independent predictor of leptin in age- and site-adjusted models (Table 5Go). After control for total percentage fat, age, and site, leptin concentrations in the black women and men were higher than in the white women and men (P < 0.001; Table 5Go, model 2). The effects of controlling for BMI or percentage fat on the difference in leptin concentrations among blacks and whites are depicted in Figures 2Go and 3Go, which show leptin concentrations stratified by decile of BMI or percentage fat, respectively. Adding abdominal visceral fat to the models in Table 5Go slightly accentuated the difference among both men and women (Table 5Go, model 3). These models predicted a higher mean leptin concentration in blacks than in whites of 4.95 ng/mL in women and 1.42 ng/mL in men. Adding additional CT measures and thigh length or thigh length-to-height ratio to the models had little effect on the race difference in leptin concentrations. Current use of oral estrogen was reported by 31% of white women and 12% of black women (P < 0.001). However, including estrogen use in the models had no significant effect on the race difference in leptin concentrations in women.


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  		TABLE 5 Relations of log serum leptin concentration (ng/mL) with race in men and women

 


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  		FIGURE 2. Geometric mean (±SE) serum leptin concentrations in men and women by BMI decile and race.

 


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  		FIGURE 3. Geometric mean (±SE) serum leptin concentrations in men and women by total percentage fat decile and race.

 

   DISCUSSION
TOP
 ABSTRACT
 INTRODUCTION
 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
REFERENCES
 
The present study confirms the strong association of total adiposity with leptin by using more precise estimates of body fatness and distribution in a large community-based biracial population of older adults. Of the body adipose measures that we studied, total percentage of fat had the highest correlation with leptin concentration. The R2 of 0.59 is similar to, or greater than, that found in other population studies that examined the correlation of percentage fat with leptin (9, 17-22). Percentage fat was the body adipose measure most highly correlated with leptin in some studies (17, 18), whereas in others total fat mass was slightly more strongly related (20-22).

Serum leptin concentrations were based on a single morning, fasting sample, but leptin concentrations have been shown to have diurnal variation and ultradian oscillations (23-25). On the basis of sex differences in leptin fluctuations, it has been suggested that women may be more resistant to the effects of leptin than are men (26) and this could help to explain the higher concentrations found in women. However, obtaining samples on multiple occasions is not possible in a population study. Furthermore, it has been shown that the use of multiple, as opposed to a single, leptin measurements does not significantly improve the relation between leptin and body fat (27). An additional limitation of the present study was that for 155 participants with leptin concentrations at the high end of the range, a numerical value was not recorded by the laboratory. We chose to recode these measurements as the value of the upper limit of the assay curve because excluding them would have resulted in a less representative sample. Furthermore, reanalyzing the data without these participants had little effect on the results.

It has been hypothesized that the sex difference in serum leptin concentrations is lessened in the elderly as the result of reduced sex hormone concentrations (28). However, in the present study of older adults, the sex difference in leptin concentrations (geometric : 16.5 and 5.7 ng/mL in women and men, respectively) was similar to that among older adults in the US population, and the sex difference in leptin concentrations varied little by decade in that population (4). Importantly, controlling for percentage body fat and abdominal visceral fat area eliminated the sex differential in leptin concentrations. Thus, among older adults, the sex difference in serum leptin concentrations appears to be explained by percentage body fat. To our knowledge, no population-based studies of leptin concentrations have looked at factors explaining sex differences specifically in older adults.

In other populations across broad age ranges, serum leptin concentrations have been consistently higher in women than in men, but whether differences in adiposity explain the sex differences in leptin concentrations is less clear. Few population-based studies of leptin concentrations have used DXA or other relatively precise techniques to measure total body fat. Similar to our findings, in a study of 766 Hispanic and non-Hispanic white adults, higher leptin concentrations in women were explained by percentage fat measured by DXA but not by total fat mass (29). In another study of 694 adults aged 21-94 y, leptin concentrations remained higher in women than in men after adjustment for total fat mass measured by DXA, but the effect of adjusting for total percentage fat was not reported (30). Both serum leptin concentration and percentage fat are ratios that may account for the stronger relation of leptin concentration with percentage fat than with total fat mass. In 2 non-population-based studies using DXA, leptin concentrations also were higher in women than in men independent of total fat mass (31, 32). In non-population-based studies in which body fat was measured by hydrodensitometry, higher leptin concentrations in women remained after adjustment for total fat mass or percentage fat (33-35). In a clinical study of older adults in which MRI was used to measure subcutaneous and visceral adipose tissue volumes, higher leptin concentrations in women than in men were incompletely explained by these factors (36). Similarly, in our population, CT measures of abdominal subcutaneous and visceral fat areas did not alone explain the sex difference in leptin concentrations.

Higher leptin concentrations in blacks than in whites could not be explained by either percentage body fat or adipose distribution. Little is known about whether variation in serum leptin concentrations by race/ethnicity is due to true differences or whether it results from limitations inherent in measuring fat. In the US population, non-Hispanic blacks had slightly but significantly higher serum leptin concentrations than did non-Hispanic whites after adjustment for anthropometric measures (4). A study from Chile found lower leptin concentrations in Mapuche natives than in Hispanics after adjustment for BMI (37), but most other population-based studies have not found major ethnic differences. Among Hispanic and non-Hispanic whites, leptin concentrations did not differ significantly after adjustment for percentage fat measured by DXA in a study in the San Luis Valley in Colorado (29). In another study, Mexican Americans had slightly but nonsignificantly higher leptin concentrations than did non-Hispanic whites after adjustment for BMI (11). Leptin concentrations did not differ among African Americans, Cuban Americans, and non-Hispanic whites after adjustment for percentage body fat calculated from waist circumference and skinfold thicknesses in a study in Dade County, Florida (9). Among non-population-based studies of leptin concentrations in African Americans and whites, findings were inconsistent (38-41).

Our inability to explain the higher leptin concentrations in the blacks in the present study may be attributable to incomplete adjustment for differences in body fat distribution. Although DXA and CT measures of body adiposity are more accurate than are the skinfold thicknesses and circumferences used in most population studies, they are still imperfect. DXA (Hologic QDR 4500A) has been found to overestimate fat-free mass and underestimate fat mass compared with a four-component model of body composition (42). However, this systematic discrepancy would account for the race difference in leptin concentrations only if the discrepancy is inconsistent by race, which it is not.

Blacks have a higher proportion of subcutaneous fat than do whites, and leptin production is higher in subcutaneous fat than in visceral fat (43, 44). Measurements of subcutaneous and visceral fat areas may incompletely account for the effects of these fat depots on leptin concentrations. Black men and women have been shown to have relatively longer lower extremities than do whites (45), which could result in variation in subcutaneous fat volumes in persons with the same subcutaneous fat areas. In the present study, adjusting for thigh length measured by CT or thigh length-to-height ratio, in addition to subcutaneous fat areas, as a crude substitute for subcutaneous fat volume had little effect on the race difference in leptin concentrations (data not shown). Hence, measurements of subcutaneous and visceral fat volumes by CT or MRI would be necessary to more fully examine the effects of race differences in specific fat depots on leptin concentrations. Alternatively, higher leptin concentrations in blacks may be due to the effects of factors other than body fat on the serum leptin concentration.

This study examined the predictors and differences in serum leptin concentrations in a large, biracial cohort of older adults. In this population, higher leptin concentrations in women resulted from a greater percentage of body fat. Higher leptin concentrations in blacks could not be explained by body fat distribution. It will be important to determine the relation of leptin to changes in body adipose tissue and health-related outcomes in this longitudinal study.


   ACKNOWLEDGMENTS
 
The contributions of the authors were as follows: CER, design and conduct of the data analysis and writing of the manuscript; JEE, Health ABC Study design, data analysis design, editing of the manuscript, advice, and consultation; JD, data analysis design and manuscript editing; BHG, Health ABC Study design and data collection, advice, and consultation; AMK, manuscript editing, advice, and consultation; EMS, Health ABC Study design and data collection, manuscript editing, advice, and consultation; FAT, Health ABC Study design and data collection, manuscript editing, advice, and consultation; TBH, Health ABC Study design and data collection, data analysis design, manuscript editing, advice, and consultation. None of the authors had a conflict of interest.


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 ABSTRACT
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 SUBJECTS AND METHODS
 RESULTS
 DISCUSSION
 REFERENCES
 

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Received for publication October 8, 2003. Accepted for publication March 3, 2004.




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