animals were fed ad libitum. Food for these groups was either a dry extruded commercial monkey diet or a commercial liquid diet for humans (Ensure®, Ross Laboratories, Columbus, OH). In analysis of the results, distinctions were not made for the diet used. Complete 3-year data sets on all animals were examined after the animals had been in the study for 9 years (Hansen et al., 1995). Remarkably, food intakes by the ad libitum and the weight-stabilized groups were relatively constant over the 3 years of data reporting; the weight-stabilized group consumed ME at an average (± SEM) of 591 ± 32 kcal·d-1 and the ad libitum group at 1,001 ± 79 kcal·d-1. Body weights were significantly different between the two groups, and these values remained relatively constant and near the mean weights (± SEM) at the age of 20 years of 11.0 ± 0.5 kg and 18.0 ± 1.5 kg in the weight-stabilized and ad libitum groups, respectively. Body fat (± SEM), estimated with the tritiated-water technique, was 21.3 ± 3.3% for the weight-stabilized group and 33.6 ± 4.0% for the ad libitum group. The energy consumed by both groups was essentially the same, ME at 54-55 kcal·kg-1 of body weight, and appeared to remain nearly constant throughout the 3 years of observation, although a trend for a slight decrease (about 10% over 3 years) was evident in the weight-stabilized group. The data indicate that the caloric intake per unit lean body mass was higher in obese than in nonobese animals (ME at 84 vs 68 kcal·BWkg-1). However, it was not established whether that represented a difference between groups in the efficiency of energy use, inasmuch as the mass of adipose tissue was over twice as great in the ad libitum group and the energy required to carry and maintain this extra weight is unknown.
Social rank among monkeys in a group may be associated with obesity (Kemnitz, 1984). The dominant animal tends to determine the time that others spend in feeding in any particular location. In captive groups, subordinate animals eat only after the dominant animal is satisfied. That pattern of hierarchic behavior might result in excessive energy intake by more dominant animals; their obesity could be partly a result of social organization. Furthermore, when social order is disrupted, as when animals co-exist in an urban environment with humans or when social groups are altered by the addition of new members, obesity might be inhibited by disruption of the dominance hierarchy. In one study of male cynomolgus macaques, disruption of social order by substitution of new monkeys for former group members was used to induce stress; although obesity was not defined, regional distribution of fat was altered in such a way that stressed monkeys accumulated more intra-abdominal fat (Jayo et al., 1993).
The distribution of body fat varies among animals. Central obesity occurs when the predominant site of adipose-tissue accumulation is the abdomen and upper body. Central obesity, typically including intra-abdominal fat accumulation, represents the distribution of adipose tissue that has been most strongly associated with defects in lipid and carbohydrate metabolism, including insulin resistance and glucoregulatory dysfunction (Kemnitz and Francken, 1986; Hansen et al., 1995), and with cardiovascular disease (Shively and Clarkson, 1988; Cefalu and Wagner, 1997) in monkeys. In a recent study (Coleman et al., 1999), adipose-tissue distribution shifted as body-weight differences increased between ad libitum-fed rhesus monkeys and diet-restricted monkeys. The percentage of body fat present in the abdomen of ad libitum-fed animals progressively increased for about 90 months of observation. At the start of the study, the average monkey weight was 11 kg, and about 40% of the body fat was in the abdomen. Ad libitumfed monkeys grew to over 14 kg, and abdominal fat increased to 45% of body fat. In contrast, the body weight of diet-restricted monkeys decreased from 11 kg to about 9 kg, and the percentage of total body fat present in the abdomen decreased to about 35%. After 90 months, the mass of total body fat was about 3 times higher in ad libitum-fed than in diet-restricted animals.
Assuming an analogy with humans, the central obesity that occurs spontaneously in rhesus monkeys appears to confer increased cardiovascular-disease risk, although measurements of cardiovascular-disease end points themselves have not been extensively studied. Hamilton et al. (1972) first reported that plasma cholesterol, triglycerides, and ß-lipoproteins were increased in obese rhesus monkeys. Hannah et al. (1991) later analyzed the plasma-lipoprotein profile and demonstrated an increase in plasma concentration of very-low-density lipoprotein cholesterol and triglycerides and a decrease in HDL cholesterol in obese, insulin-resistant rhesus monkeys. Both those changes in lipoproteins would tend to increase the risk of coronary heart disease. Conversely, by inhibiting the development of obesity with diet restriction, Edwards and co-workers (1998) showed that, although LDL cholesterol concentrations were unchanged, LDL particles were modified in composition and had a decreased tendency to interact with arterial proteoglycans. Diet restriction thus appeared to block one of the proposed mechanisms of atherosclerosis, or ‘‘hardening of the arteries’’, in which LDL particles are trapped in the arterial intima and effectively stimulate inflammatory responses. No direct measurements of atherosclerosis have been reported in obese, diabetic rhesus monkeys, although experimental atherosclerosis in this species has been well characterized (Armstrong, 1976). The use of Western (fat-and cholesterol-enriched) diets to induce hyperlipidemia is a prerequisite for promoting the development of atherosclerosis, and the likelihood that effects of obesity on atherogenesis will be observed in the absence of this dietary background seems small. Most of the studies on obesity have not used this type of diet.