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Nutrient Requirements of Nonhuman Primates: Second Revised Edition, 2003
Four infant crab-eating macaques (M. fasicularis), 5-7 months old, also were fed a 2% casein diet over 14 weeks (Worthington et al., 1979) and exhibited significant decreases in plasma essential amino acids (especially the branched-chain group), whereas plasma nonessential amino acids tended to rise (especially glycine and alanine). The peak response was noted within 3-4 weeks of protein restriction.
Nine 6- to 9-month-old male crab-eating macaques (M. nemestrina) from the study of Enwonwu et al. (1977) were later further diet-restricted and fed the 20% and 2% casein diets at 200 g·day-1 for 20 weeks to examine hepatic alterations associated with PCM. Mean initial BW of both groups was 1.4 ± 0.13 kg. Control monkeys fed the 20% casein diet showed a 40% net gain of BW during the 20-week study. Monkeys receiving the 2% casein diet showed a 4% net gain of BW, which was consistent with marked accumulation of extracellular fluid. Severe disturbances of the structure and function of the liver were noted.
Female rhesus macaques (M. mulatta), 12-24 months old and weighing 2.1 to 3.0 kg, were fed either 2% or 0% protein diets (isocaloric to 20% casein diet) to provide undefined energy at 100 kcal·BWkg-1·day-1. Structural changes were observed in the liver, myocardium, and striated muscle. There also was extensive cytoplasmic necrosis of the pancreas, the organ most severely affected; and cellular injury was evident in pancreatic secretions that were enzyme-deficient (Racela et al., 1966). In kwashiorkor, pancreatic enzymes have been described as deficient at a very early stage of the disease before fatty change of the liver is evident. During a 6-week interval, six 4-kg rhesus macaques (M. mulatta) were fed a diet deficient in protein but providing undefined energy at 100 kcal·BWkg-1·day-1. They developed carbohydrate intolerance attributed to diminished insulin production, hepatic dysfunction, and decreased glucose disposal as a consequence of protein deprivation (Khardori et al., 1980).
Young squirrel monkeys (Saimiri sciureus, Leticia) have been used as pediatric models in malnutrition studies because they share several physiologic characteristics with human infants. They were fed diets restricted in protein, in energy, or in both (Gallina et al., 1987; Ausman et al., 1989) from the age of 2 to 8 weeks, or were only protein-restricted from the age of 4 to 24 weeks (Gallina et al., 1987) to support maintenance of BW without significant weight gain. The earlier study was designed to investigate the effects of particular nutritional deficiencies on plasma concentrations of albumin and transferrin, proteins used as biochemical indexes of nutritional status. Imposition of severe energy restriction (less than 250 kcal ME·BWkg-1· day-1) with adequate protein intake (23% of calories) did not lower serum albumin concentrations in four animals— a finding similar to that observed in another ceboidea species (Cebus albifrons) fed similarly (Samonds and Hegsted, 1978). Plasma albumin levels were decreased only when dietary protein (6.82% or 3.41% of calories), but not energy, was low (Gallina et al., 1987). Plasma transferrin in the control animals was significantly higher than in animals that were diet-restricted in protein, energy, or both. Sixteen monkeys exhibited an adaptive response to dietary manipulation in which energy restriction (288 ± 30 kcal ME·BWkg-1·day-1 vs control 449 ± 71 kcal ME·BWkg-1· day-1) coupled with protein restriction (4.9 ± 0.3 g·BWkg-1 ·day-1 vs control 14.6 ± 2.3 g·BWkg-1·day-1) provided no evidence of a more severe protein deficiency than protein restriction alone (Ausman et al., 1989).
The effects of PCMon early growth of 8- to 28-week-old, 520-g cebus monkeys (Cebus albifrons) were studied when they were fed a synthetic liquid control diet (13% of calories as lactalbumin protein and undefined energy at 135 kcal·day-1), a low-protein diet (2.8% of calories), or a low-calorie diet (90 kcal·day-1) (Fleagle et al., 1975). By week 4 of the 20-week study, significant body-size differences were apparent. By 20 weeks, both protein- and calorie-restricted animals had developed a thin, emaciated appearance associated with marasmus, not from continuous loss of tissue but from redistribution of tissue over a slowly expanding skeleton that differed in proportion and shape from that of control monkeys. Fatty liver also was associated with a low protein concentration or dietary amino acid imbalance in cebus and rhesus (M. mulatta) monkeys (Wilgram et al., 1958).
Sucrose, when provided as the primary carbohydrate— 20% of the total energy in a low-protein diet—potentiated the development of fatty liver, a rapid fall in serum albumin concentration to 1 g·dl-1, edema, and other signs of kwashiorkor among young baboons (Papio spp.). These baboons were diet-manipulated (low-protein, high-carbohydrate staples: banana, cassava, and matooke) and periodically stressed with acute energy restriction to produce models of PCM(Coward and Whitehead, 1972). Average protein and undefined energy intakes of control baboons were 6.1 g·BWkg-1· day-1 and 290 kcal·BWkg-1·day-1, respectively. Average serum albumin concentrations in the controls were maintained at 4.05 g·dl-1. When starch was the primary carbohydrate, there was a notable absence of fatty liver infiltration among similar baboons (Coward and Whitehead, 1972; Whitehead, 1980). Suppressed immune response in three baboons with signs of kwashiorkor also has been reported (Qazzaz et al., 1981).
Marmosets and tamarins, members of the family Callitrichidae, also have served as nonhuman-primate models of human disease. In research laboratories, they have suffered reproductive inefficiencies and high mortality due to the occurrence of “wasting marmoset syndrome” (WMS), a protein-calorie deficiency that is characterized by weight loss, alopecia, chronic diarrhea, muscle atrophy, chronic