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The Journal of Nutrition Vol. 128 No. 2 February 1998,
pp. 390S-393S
Division of Nutritional Sciences, Cornell University, Ithaca, NY 14853
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ABSTRACT |
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To study the effects of maternal nutritional status on lactational performance, the diets of laboratory rats were manipulated with food restriction or increases in fat concentration. Compared with rats fed control diets ad libitum, conception rate, milk production and litter growth decreased and milk fat concentration increased in both chronically food restricted and obese animals. Chronically food restricted rats mobilized body fat and reduced their energy expenditure for maintenance and activity. Differences in suckling pattern between control and food-restricted rats affected hormone concentrations important for successful lactation. Obese rats experienced greater difficulty than controls in delivering their pups and more of their pups died in the first days of life. Milk production among obese rats may be constrained by poor appetite and the high heat production that characterizes lactation in litter-bearing species. There are many parallels as well as important differences between results obtained from these models and findings in nursing women. Nevertheless, these models provide useful information about the possible mechanisms by which maternal nutritional status affects lactational performance.
KEY WORDS: undernutrition · obesity · rats · lactation · milk
It has long been recognized that women who are extremely thin or fat have difficulty conceiving and that this problem can be cured by modifying their weight to a more normal value (Mitchell and Rogers 1953 Animal models of protein-energy malnutrition differ primarily in the severity and timing of the deficiency. The most common approach is to offer animals a reduced proportion of the usual diet. In studies of lactation, this dietary treatment is usually imposed at parturition (acute food restriction) or several weeks before mating (chronic food restriction). Acute food restriction is a model in which dietary inadequacy is imposed during an established reproductive state and, because the animal has a reduced ability to adapt to this condition, it simulates famine conditions in a previously well-nourished population. In contrast, chronic food restriction is a model in which the stress of reproduction is imposed on an animal previously adapted to chronic food insufficiency. As such, it is a model for the conditions commonly seen in developing countries in which women of reproductive age are stunted in response to a condition of inadequate food intake that has existed since childhood.
Two different dietary approaches for producing obesity in laboratory rats have been used to study the effects of maternal overnutrition on lactational performance. With "cafeteria feeding," rats are offered a selection of high fat, highly palatable foods in addition to their usual closed-formula diet. This is a reasonable model for human dietary patterns, but it is difficult to know exactly what the rats have consumed, and they may choose a diet that may not contain sufficient protein for reproduction.
It is clear from comparison of the results from these models in laboratory rats of under- and overnutrition that maternal nutritional status both before and during lactation exerts a profound effect on lactational performance. This can be seen in the combined data on carcass fat content at d 20 of pregnancy and d 14 of lactation (Fig. 1), pup birthweight and weight gain during the first 14 d after birth (Fig. 2) and milk volume and lipid concentration at d 14 of lactation (Fig. 3) from food-restricted rats, control rats and those fed a high fat diet. Furthermore, this effect of maternal nutritional status on lactation performance is probably not limited to nutrient flux during lactation (Rasmussen 1992 The contributions of Miriam Alexander, Heather Brigham-Matthews, Karen Fischbeck, Michelle McGuire, Tami Myers, Rebecca Kliewer Olson, Helena Pachón, Tami Sakanashi, Maureen Shaw, Mary Wallace and Carolyn Young to the work reported here are gratefully acknowledged.
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INTRODUCTION
Abstract
Introduction
References
). This suggests that there is a body weight and/or composition associated with optimal reproductive success. Researchers have focused on body fatness as the key aspect of body composition meriting investigation. The specific optimum body characteristics may differ for each reproductive outcome. This principle has not been applied previously to lactation, particularly with data from states of both under- and overnutrition.
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MODELS OF UNDERNUTRITION
DURING LACTATION
) and a 32% reduction in litter weight (Kliewer and Rasmussen 1987
) at d 14 of lactation. The primary change in milk composition is a reduction in lactose concentration (Brigham et al. 1992
, Kliewer and Rasmussen 1987
). Dams subjected to acute food restriction lose weight during lactation (Brigham et al. 1992
, Kliewer and Rasmussen 1987
) and have higher concentrations of plasma corticosterone than control animals (Kliewer and Rasmussen 1987
). The proportion of cardiac output that is directed to the mammary glands, and both absolute and relative blood flow to the mammary glands are reduced in these rats (Sakanashi et al. 1987
).
) and fewer liveborn pups are delivered (Young and Rasmussen 1985
); dams gain less weight during pregnancy (Young and Rasmussen 1985
). Carrying fewer pups to term permits food-restricted dams to protect the weight of individual pups (Rasmussen and Fischbeck 1987
, Young and Rasmussen 1985).

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Fig 1.
Effect of chronic dietary treatment on carcass fat concentration at d 20 of pregnancy (P) and d 14 of lactation (L). Sources: Young and Rasmussen (1985)
, Wallace, M. H. and Rasmussen, K. M., unpublished data.
) and a 61% reduction in litter weight (Kliewer and Rasmussen 1987
) at d 14 of lactation. Milk lactose concentration decreases and fat concentration increases in dams subjected to chronic food restriction; as a result, the caloric density of their milk tends to increase (Brigham et al. 1992
, Kliewer and Rasmussen 1987
), but not enough to compensate for the large reduction in milk volume. Body weight decreases minimally during lactation in dams subjected to chronic food restriction. Their plasma corticosterone concentrations are increased and prolactin concentrations decreased compared with controls (Kliewer and Rasmussen 1987
).
). When dietary restriction begins before conception, food-restricted dams are smaller than controls, and some of their reduced energy expenditure for maintenance during lactation results from their smaller body size (Sadurskis et al. 1991
). Food-restricted rats mobilize more body fat and produce less milk than controls (Sadurskis et al. 1991
).
), but has the advantage of revealing effects that might otherwise be too small to detect in reasonable numbers of human subjects.
). This likely results from differences between women and these rats in the severity of food restriction. At 50% of ad libitum intake, rat dams search for food instead of nursing their pups. In contrast, rats restricted to 70% of ad libitum intake have increased prolactin values (McGuire et al. 1995
). This lesser degree of food restriction is more similar to that characteristic of poorly nourished human populations.
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MODELS OF OVERNUTRITION DURING LACTATION

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Fig 2.
Effect of chronic dietary treatment on pup weight at birth (left) and daily gain from birth to d 14 (right). HF is high fat and C* (AIN-76) and C** (AIN-93) are different control dietary treatment groups; ***, significantly different (P < 0.05) from C** group. Sources: Young and Rasmussen (1985)
, Wallace and Rasmussen, unpublished data.

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Fig 3.
Effect of chronic dietary treatment on milk production (left) and lipid concentration at d 14 of lactation (right). HF is high fat and C* (AIN-76) and C** (AIN-93) are different control dietary treatment groups. Sources: Young and Rasmussen (1985)
, Wallace and Rasmussen, unpublished data.
, Shaw et al. 1997
). These animals will be described as "obese" (although no formal standard exists by which to classify them this way). Obese rats suffer from estrous cycle irregularities (Glick et al. 1990
), may not conceive as readily as controls (Wallace M. H. and Rasmussen K. M., unpublished data) and implant fewer embryos (Shaw et al. 1997
). They gain weight less readily near term (Shaw et al. 1997
) or they may gain less weight overall (Wallace and Rasmussen, unpublished data). Obese rats deliver fewer and lighter pups than controls (Wallace and Rasmussen, unpublished data) and are more likely to have difficulty delivering; their pups are much more likely to die in the first few days after birth (Rolls et al. 1980
, Shaw et al. 1997
, Wallace and Rasmussen, unpublished data). Inasmuch as many of the pups who die have no visible milk in their stomachs, inadequate initiation of lactation is a possible cause of death. Our observational data are inadequate to exclude inappropriate maternal behavior as an additional, contributing cause.
, 1983 and 1986, Wallace and Rasmussen, unpublished data). Pups who survive do not grow as well as pups of control rats (Wallace and Rasmussen, unpublished data). Obese rats do not develop the hyperphagia that is characteristic of lactation in the rat (Rolls et al. 1980
). Milk production is not limited by mobilization of maternal caloric reserves because obese dams lose more weight and fat during lactation than controls; nonetheless, they remain fatter at d 14 of lactation (Wallace and Rasmussen, unpublished data).
).
) suggest that this supports higher milk production and pup growth. However, other investigators (Guo and Jen 1995
) have identified deleterious effects of maternal high fat feeding on the metabolism of these larger pups (higher blood glucose and triglyceride concentrations).
). Lipogenesis increases in brown adipose tissue (Agius et al. 1981
). Glucose uptake, and lipogenesis (Agius et al. 1980
) and acetyl-CoA carboxylase activity (Munday and Williamson 1987
) are reduced in isolated acini from mammary glands of rats fed a cafeteria diet. Dams fed high fat diets become ketotic (Agius et al. 1983
), which decreases appetite (Friggens et al. 1993
). It is also possible that their food intake is constrained because their heat production is already maximal (Friggens et al. 1993
).
, Rutishauser and Carlin 1992
), but it appears that the laboratory rat is an adequate animal model for studying this issue because of the parallels in physiologic findings that have been identified to date.
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LINKING FINDINGS ACROSS THE SPECTRUM OF MATERNAL NUTRITIONAL STATUS
). The studies cited here reveal effects of maternal nutritional status on mammary gland development, rates of conception, implantation and fetal survival. Metabolic and endocrinologic changes at and after parturition are also important. The results of these studies extend to lactation the principle that extremes of maternal nutritional status are associated with adverse outcomes.
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ACKNOWLEDGMENTS
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FOOTNOTES |
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LITERATURE CITED |
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