AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 89:109-121 (1992)

Age- and Gender-Related Changes in Body Size, Adiposity, and Endocrine and Metabolic Parameters in Free-Ranging Rhesus Macaques SUSAN M.SCHWARTZ AND JOSEPH W.KEMNITZ Caribbean Primate Research Center and Department of Obstetrics1 Gynecology, University of Puerto Rico, Medical Science Campus, Sun Juan, Puerto Rico 00936 (S.M.S.); Wisconsin Regional Primate Research Center, University of Wisconsin, Madison, Wisconsin 53715 (J.W.K.)

KZY JVORDS Macaca muiatta, Adiposity, Lipids, IGF-1, Obesity, Aging, Cay0 Santiago ABSTRACT Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the Cay0 Santiago free-ranging rhesus macaques. In both adult males and females, body weights, crown-rump lengths, and circumference of the limbs were lowest in the oldest group (20+ years of age) as compared with other adult age classes. Body fat, as reflected in subcutaneous fatfold thickness and waistfthigh ratios, were higher in adult females than adult males. This gender dimorphism was first detectable among the 6-9 year old age group. Greatest body fat among females was observed in the 10-14 age group, whereas in males the highest values were observed in the 15-19 age group. Differences in body composition were also observed with respect to reproductive status. Although there were no gender differences in overall cholesterol levels, there were age-related differences between males and females, and only in males were cholesterol values positively related to adiposity. There were no age- or gender-related differences in triglyceride values, but levels were significantly higher in pregnant females in comparison with other reproductive states. Levels of testosterone were not significantly related t o any morphometric parameter and values did not decrease significantly with age. Levels of IGF-1 exhibited a significant age-related decrease among adult males, and females had higher levels independent of age. The similarities between the present findings and human studies suggest that further studies in the free-ranging rhesus macaques would provide a bridge between studies of laboratory-housed primates and studies of human beings with respect to the etiology of obesity and life-history changes in body composition and endocrine and metabolic parameters. o 1992 Wiley-Liss, Inc. Information on body size, adolescent growth, and development of gender dimorphisms has been documented in several captive colonies of rhesus macaques (Schultz, 1956; van Wagenen and Catchpole, 1956; Gavan and Hutchinson, 1973; Watts and Gavan, 1982; Goy and Kemnitz, 1983; Kenmitz et al., 19881, with morphometric data recently reported for the Cay0 Santiago population (Turnquist and Kessler, 1989). However, information on age- and gender0 1992 WILEY-LISS,INC.

related changes in body composition, particularly body fat, are unavailable. Data on normative somatic patterns among freeranging nonhuman primates might provide valuable insights into the developmental sequence of growth and metabolic disease in human beings. Indirect analysis of body composition is assessed through various anthropometric Received February 27,1991; accepted March 9,1992

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measurements. Ratios of body weight in relation to height have been developed for the human population of which the body mass index (BMI; body weight divided by the square of the height) is best correlated with total body fat (Bray, 1987). Circumference and skinfold measurements are used to provide insight into regional fat distribution. For example, the ratio of the circumference of the waist to the circumference of the hips, the waist-hips ratio (WHR),is an important predictor of risk associated with obesity (Bray, 1387). Similar techniques ha.ire been used to assess obesity in macaques (Walike et al., 1977; Kemnitz, 1984; Walker et al., 1984; Jen et al., 1985; Leathers, 1985; Kemnitz and Francken, 1986).Abdominal fatfold (Walike et al., 1977; Walker et al., 1984), BMI (Jen et al., 1985) or abdominal circumference (Kemnitz and Francken, 1986; Kemnitz et al., 1989) are reliable predictors of percent body fat as directly determined through radioisotope methods. Moreover, a similar ratio to WEIR, the ratio of the circumference of the abdomen to the circumference of the thigh (wsthhigh ratio), is highly correlated with body fat in rhesus macaques (Kemnitz et al., 1989). Indices such as chest and upper-arm circumference, on the other hand, are good predictors of lean body mass (Kemnitz et al., 1988). A limitation with these data is most measurements have been collected from obese monkeys; baseline information from normal, well-nourished animals is limited and does not encompass the entire life span of the individual (Coehlo, 1985). In both human beings and nonhuman primates, a number of metabolic and endocrine factors are associated with changes in fat distribution. Serum lipids such as cholesterol and triglyceride are positively related to body fat distribution in obese (Albrink et al., 1980; Matter et al., 1980) and nonobese individuals (Despres et al., 19881, and elevated levels of lipids and lipoproteins have been documented in obese rhesus macaques (Hamilton et al., 1972; Kemnitz and Francken, 1986; Hansen, 1987; Hannah et al., 1991). Gender differences in these lipids have been observed, with lower levels observed in women despite a greater percent body fat (Despres et al., 1985). Gonadal hor-

mones are also influenced by adiposity. There are obesity-related changes in androgen and estrogen metabolism in both men and women (Bates and Whitworth, 1982; Schneider et al., 1979). Decreases in testosterone levels have been reported in obese men (Glass et al., 1977; Kley et al., 1980) as well as in older men (Vermeulen et al., 1972; Pirke and Doerr, 1973; Stearns et al., 1974, but see Coppage and Conner, 1965; Harmon and Tsitouras, 1980); similar obesity-related decreases occur in laboratory-housed male rhesus macaques (Kemnitz et al.. 1989). Information on normative patterns for these metabolic and endocrine factors in relation to body composition might provide insight into the effects of age and gender on obesity-related metabolic abnormalities. A number of alterations in body composition are associated with human aging including a decrease in lean body mass (Cohn et al., 1980), an increase in total and central deposition of body fat (Cohn et al., 1980; Shimokata et al., 1989; Borkan and Norris, 19771, and changes in bone density (Parfitt, 1983; Mazess and Cameron, 1975). Aging is also associated with changes in the production and utilization of growth-related hormones such as growth hormone (GH) and insulin-like growth factor (IGF-1). Concentrations of both GH and IGF-1, a polypeptide that mediates the anabolic effect of GH, are lower in elderly people (Hammerman, 1987; Pavlov et al., 1986; Rudman, 1985: Rudman et al., 1990) and decreases in GH have been observed with advancing age in adult male rhesus macaques (Wheeler et al., 1990). Decreased concentrations of GH also have been documented in both obese human beings and monkeys (Glass et al., 1981; Meistas et al., 1982; Dubey et al., 19881,and an inverse association of adiposity with IGF-1, independent of age, has been reported in the human population (Rudman et al., 1981; Copeland et al., 1990). The relationship between age-related somatic changes and IGF-1 has not been examined in nonhuman primates. The aim of the present study was to document age- and gender-related somatic patterns in association with changes in adiposity and with potential biochemical and endocrine correlates. In providing a perspec-

SOMATIC PATTElINS IN MONKEYS

tive into factors contributing to the development of obesity, the data also add to our understanding of life history changes in morphometric, endocrine, and biochemical parameters among free-ranging nonhuman primates. Although the design is not longitudinal, a relatively large cross-sectional sample of the population is used to infer longitudinal somatic changes (Coehlo, 1985).

MATERIALS AND METHODS Subjects and methods

The rhesus macaque (Macaca mulatta) colony of Cay0 Santiago was established in 1938 (Rawlins and Kessler, 1986). New animals have not been introduced into the colony, but monkeys are removed periodically from the island t o prevent overpopulation. Although some secular trends in body size and proportion have occurred in this colony (DeRousseau and Reichs, 19871, resources and conditions of the island have remained relatively stable over the life span of animals encompassed by the study. Monkeys on the island are provisioned with approximately 0.25 kg per animal per day of commercial high protein (26%) diet (Agway Inc., Syracuse, NY),with 12%of calories derived from fat. Monkeys generally eat in the morning at one of three large feeding areas located within fenced corrals in conjunction with their social troop, but additional feedings by individuals, particularly peripheral adult mates, are common Animals also spend significant amounts of time foraging on natural vegetation (Marriott et al., 1989).Water is available ad libitum from gravity-fed fountains dispersed throughout the island. During 1988 and 1989 the population was organized into seven social groups and a small group of peripheral males who were not affiliated with any troop. Eleven matrilines, all of which can be traced back to 1956 (Altmann, 1962), were present when the current study was begun. Monkeys are captured annually in January for health surveillance and for collection of demographic and biomedical data. A total of 326 animals were examined during 1988 (n = 150) and 1989 (n = 1761, representing

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approximately 16%of the annual population and 32% of the adult population. The monkeys surveyed ranged in age from infancy to 29 years, but emphasis was placed on capturing adult animals. Most animals were captured either when their social group entered the corrals to feed, but some were individually darted with ketamine HCI. A number of animals were food deprived for 12-20 hours by placing them in individual cages overnight. Data were collected while animals were sedated (ketamine HC1; 12 mgkg bodv weight). Measurements on infants (4weeks) were made without chemical restraint and included only body weights and crown-rump length. Body weights were collected on a digital scale accurate to 0.01 kg. Crown-rump length was measured with the monkey in left lateral recumbancy using Vernier Anthropometric calipers accurate to 0.1 cm. Circumference for the mid-upper arm (triceps), mid-upper leg (thigh), chest (at the level of the nipples), and abdomen (at the level of the umbilicus) were collected with a tape measure to the nearest 0.1 cm. Measurements of the mid-thigh were not obtained from all adult animals in 1988 (n = 72). Subcutaneous fat depth was measured to the nearest 1.0 mm with a Lange caliper at scapular and abdominal (2 cm above and 2 cm below the umbilicus) sites. The BMI was calculated as body weight (kg)lcrownrump length (rn),. Waisthhigh (wstlth: abdominal circumferencelthigh circumference), waisttlength (bulge; abdominal circumference/crown-rump length), and waisti chest (sag; abdominal circumferencelchest circumference) ratios were calculated. These ratios have been used as indicators of body fat distribution in rhesus macaques (Leathers, 1985; Kemnitz et al., 1989). Serum was collected from animals in 1988 for determination of cholesterol (n = 70) and triglycerides (n = 72). Levels of estradiol (E,) and testosterone (T)were measured in a number of males (n = 56) and IGF-1 levels were examined in selected animals (n = 26). All samples were collected in the morning to control for diurnal effects. Total cholesterol and triglycerides were determined in fasted samples using colorimetric procedures (Diagnostic Chemicals, Limited, Canada). Se-

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rum T and E2 concentrations were determined using commercially prepared reagents (Diagnostic Products Corp., Los Angeles). For the E2 assay, rather than using human serum as the diluent, serum from gonadectomized monkeys was treated with charcoal to remove any residual steroids and was used as the diluent. IGF-1 concentrations were obtained by RIA following a 48-hr acid treatment of serum, as described previously (Osterud et al., 1986). Both intra and interassay coefficients of variation for all RE4 procediires werc

Age- and gender-related changes in body size, adiposity, and endocrine and metabolic parameters in free-ranging rhesus macaques.

Normative age- and gender-related changes in body composition, serum lipids, testosterone, and insulin-like growth factor (IGF-1) were examined in the...
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