Abstract
Early malnutrition may be considered a maternal manipulation: the mother is directly affected by the malnutrition, whereas the offspring are affected by the maternal response to malnutrition. In spite of an extensive literature in the area of early malnutrition, particularly its implications for neural and behavioral development (e.g., Dobbing, 1984; Leathwood, 1978; Zamenhoff & Van Marthens, 1978), few have attempted to address the basic question of what nutrients get through to the fetus and the neonate. In rats, we know what we feed to the dams, either pregnant or lactating. Do we know what nutrients the pups get? The answer to this question is largely negative. Ignorance of the actual proximal effects of malnutrition can lead us astray, for example, when we compare postnatal to prenatal malnutrition. In such comparisons, both the nutrients available to the offspring and their developmental stage differ.
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Ahokas, R. A., Anderson, G. D., & Lipshitz, J. Cardiac output and uteroplacental blood flow in diet-restricted and diet-repleted pregnant rats. American Journal of Obstetrics and Gynecology, 1983, 146, 6–13. (a)
Ahokas, R. A., Anderson, G. D., & Lipshitz, J. Effect of dietary restriction during the last week only or throughout gestation, on cardiac output and uteroplacental blood flow in pregnant rats. Journal of Nutrition, 1983, 113, 1766–1776.(b)
Battaglia, F. C. Energy and substrate requirements for fetal and placental growth and metabolism. In R. W. Beard & P. W. Nathanielsz (Eds.), Fetal physiology and medicine. New York: Marcel Dekker, 1984.
Berg, B. N. Dietary restriction and reproduction in the rat. Journal of Nutrition, 1965, 87, 344–350.
Blackwell, B. N., Blackwell, R. Q., Yu, T. T. S., Weng, Y. S., & Chow, B. F. Further studies on growth and feed utilization in progeny of underfed mother rats. Journal of Nutrition, 1969, 97, 79–84.
Bruce, N. W. The effect on fetal development and utero-placental blood flow of ligating a uterine artery in the rat near term. Teratology, 1977, 16, 327–332.
Burd, L. I., Jones, M. D., Simmons, M. A., Makowski, E. L., Meschia, G., & Battaglia, F. C. Placental production and foetal utilisation of lactate and pyruvate. Nature, 1975, 254, 710–711.
Burt, R. L., Leake, N. H., & Rhyne, A. L. Human placental lactogen and insulin-blood glucose homeostasis. Obstetrics and Gynecology, 1970, 36, 233–237.
Bush, M., & Leathwood, P. D. Effects of differing regimens of early malnutrition on behavioral development and adult avoidance learning in Swiss white mice. British Journal of Nutrition, 1975, 33, 373–385.
Butler, S. R., Suskind, M. R., & Schanberg, S. M. Maternal behavior as a regulator of polyamine biosynthesis in brain and heart of the developing rat pup. Science, 1978, 199, 445–447.
Capek, K., & Jelinek, J. The development of the control of water metabolism: I. The excretion of urine by young rats. Physiologia Bohemoslovaca, 1956, 5, 91–96.
Chow, B. F., & Lee, C. J. Effect of dietary restriction of pregnant rats on body weight gain of the offspring. Journal of Nutrition, 1964, 82, 10–18.
Costrini, N. V., & Kalkhoff, R. K. Relative effects of pregnancy, estradiol, and progesterone on plasma insulin and pancreatic islet insulin secretion. Journal of Clinical Investigation, 1971, 50, 992–999.
Cowley, J. J., & Griesel, R. D. The development of second-generation low-protein rats. The Journal of Genetic Psychology, 1963, 103, 233–242.
Crawford, M. A., Hassam, A. G., Williams, G., & Whitehouse, W. L. Essential fatty acids and fetal brain growth. Lancet, 1976, 1, 452–453.
Crnic, L. S. Models of infantile malnutrition in rats: Effects on maternal behavior. Developmental Psychobiology, 1980, 13, 615–628.
Crnic, L. S. Effects of nutrition and environment on brain biochemistry and behavior. Developmental Psychobiology, 1983, 16, 129–145.
Crnic, L. S. Unpublished observations, 1978.
Crnic, L. S., & Chase, H. P. Models of infantile undernutrition in rats: Effects on milk. Journal of Nutrition, 1978, 108, 1755–1760.
Croskerry, P. G., & Smith, G. K. Thermoregulation and the nesting behaviour of the rat. Nature, 1978, 273, 299–300.
Dancis, J. The placenta: An overview. In U. Stave (Ed.), Perinatal physiology. New York: Plenum Press, 1978.
Dayton, D. H., Filer, L. J., & Canosa, C. Cellular changes in placentas of undernourished mothers in Guatemala. Federation Proceedings, 1969, 28, 488–492.
Deguchi, T. Circadian rhythm of enzyme and running activity under ultradian lighting schedules. American Journal of Physiology, 1977, 232, E375–E381.
Dobbing, J. Vulnerable periods in the developing brain. In A. N. Davidson & J. Dobbing (Eds.), Applied neurochemistry. Philadelphia: F. A. Davis, 1968.
Dobbing, J. Infant nutrition and later achievement. Nutrition Reviews, 1984, 42, 1–7.
Ellinger, G. M., Duckworth, J., Dalgarno, A. C., & Quenouille, M. H. Skeletal changes during pregnancy and lactation in the rat: Effect of different levels of dietary calcium. British Journal of Nutrition, 1952, 6, 235–253.
Fleischer, S. F., & Turkewitz, G. Behavioral effects of rotation between lactating and nonlactating females. Developmental Psychobiology, 1981, 12, 245–254.
Fleming, A. S. Control of food intake in the lactating rat: Role of suckling and hormones. Physiology and Behavior, 1976, 17, 841–848.
Frazier, J. F. D., & Huggett, A. The partition of nutrients between mother and conceptus in the pregnant rat. Journal of Physiology, 1970, 207, 783–788.
Freinkel, N., Metzger, B. E., Nitzan, M., Hare, J. W., Shambaugh, G. E., Marshall, R. T., Surmaczynska, B. Z., & Nagel, T. C. “Accelerated starvation” and mechanism for the conservation of maternal nitrogen during pregnancy. Israeli Journal of Medical Science, 1972, 8, 426–439.
Friedman, M. I. Effects of milk consumption and deprivation on body fluids of suckling rats. Physiology and Behavior, 1979, 23, 1029–1033.
Galler, J. R., & Turkewitz, G. Use of partial mammectomy to produce malnutrition in the rat. Biology of the Neonate, 1977, 31, 260–265.
Gilbert, M., & Leturque, A. Fetal weight and its relationship to placental blood flow and placental weight in experimental intrauterine growth retardation in the rat. Journal of Developmental Physiology, 1982, 4, 237–246.
Goy, R. W., & McEwen, B. S. Sexual differentiation of the brain. Cambridge: M.I.T. Press, 1980.
Gruenwald, P., & Minh, H. N. Evaluation of body and organ weights in perinatal pathology. American Journal of Obstetrics and Gynecology, 1961, 312, 312–320.
Grumbach, M. M., Kaplan, S. L., Sciarra, J. J., & Burn, I. M. Chorionic growth hormone-prolactin (CGP): Secretion disposition, biologic activity in man, and postulated function as the “growth hormone” of the second half of pregnancy. Annals of the New York Academy of Science, 1968, 148, 501–531.
Hall, R. D., Leahy, J. P., & Robertson, W. M. The effect of protein malnutrition on the behavior of rats during the suckling period. Developmental Psychobiology, 1979, 12, 455–466.
Hall, W. G., & Rosenblatt, J. S. Developmental of nutritional controls of food intake in suckling rat pups. Behavioral Biology, 1978, 24, 412–427.
Hall, W. G., Cramer, C. P., & Blass, E. M. Ontogeny of sucking in rats: Transitions toward adult ingestion. Journal of Comparative and Physiological Psychology, 1977, 91, 1141–1155.
Hay, W. W., Jr., Sparks, J. W., Quissell, B. J., Battaglia, F. C., & Meschia,G. Simultaneous measurements of umbilical uptake, fetal utilization rate, and fetal turnover rate of glucose. American Journal of Physiology, 1981, 240, E662–E668.
Hay, W. W., Jr., Sparks, J. W., Battaglia, F. C., & Meschia, G. Maternal-fetal glucose exchange: Necessity of a three pool model. American Journal of Physiology, 1984, 246, E528–E534.
Heim, T., & Szelenyi, Z. Temperature regulation in rats semi-starved since birth. Acta Physiologica, 1965, 27, 247–255.
Hennessy, M. B., Laughlin, N. K., Wiener, S. G., & Levine, S. Malnutrition and maternal behavior in the rat. In R. W. Bell & W. P. Smotherman (Eds.), Maternal influences and early behavior. New York: SP Medical and Scientific Books, 1980.
Henning, S. J., Chang, S. S. P., & Gisel, E. G. Ontogeny of feeding control in suckling and weanling rats. American Journal of Physiology, 1979, 237, R187–R191.
Hofer, M. A., & Weiner, H. Physiological mechanisms for cardiac control by nutritional intake after early maternal separation in the young rat. Psychosomatic Medicine, 1975, 37, 8–24.
Hummel, L., Schirrmeister, W., & Wagner, H. Quantitative evaluation of the maternal-fetal transfer of free fatty acids in the rat. Biology of the Neonate, 1975, 26, 263–267.
Hytten, F. E., & Paintin, D. B. Increase in plasma volume during pregnancy. Journal of Obstetrics and Gynaecology of the British Commonwealth, 1963, 70, 402–409.
Iyengar, L. Urinary estrogen excretion in undernourished pregnant Indian women. American Journal of Obstetrics and Gynecology, 1968, 102, 834.
Jones, A. P., & Friedman, M. I. Obesity and adipocyte abnormalities in offspring of rats undernourished during pregnancy. Science, 1982, 215, 1518–1519.
Jones, A. P., Simson, E. L., & Friedman, M. I. Early gestational undernutrition and the development of obesity in rats. Journal of Nutrition, 1984, 114, 1484–1492.
Jones, C. T., & Parer, J. T. The effect of alterations in placental blood flow on the growth of the nutrient supply to the fetal guinea-pig. Journal of Physiology, 1983, 343, 525–537.
Josimovich, J. B., & Archer, D. F. The role of lactogenic hormones in the pregnant mother and fetus. American Journal of Obstetrics and Gynecology, 1977, 129, 770–780.
Keen, C. L., Lonnerdal, B., Clegg, M., & Hurley, L. S. Developmental changes in composition of rat milk: Trace elements, minerals, protein, carbohydrate and fat. Journal of Nutrition, 1981, 111, 226–230.
Kim, Y. J., & Felig, P. Plasma chorionic somatomammotropin levels during starvation in mid pregnancy. Journal of Clinical Endocrinology and Metabolism, 1971, 32, 864–866.
Knittle, J. L., & Hirsch, J. Effect of early nutrition on the development of rat epididymal fat pads: cellularity and metabolism. Journal of Clinical Investigation, 1968, 47, 2091–2098.
Knopp, R. H., Borousb, M. A., & O’Sullivan, J. B. Lipid metabolism in pregnancy: II. Post heparin lipolytic activity and hypertriglyceridemia. Metabolism, 1975, 24, 481–485.
Kohler, E., Wojnorowicz, F., & Borner, K. Effects of a protein-free diet on amino acids and sex hormones of rats during early post-implantation stages of pregnancy. Journal of Reproduction and Fertility, 1975, 42, 9–21.
Kumerasan, P., Anderson, R. P., & Turner, C. W. Effect of litter size upon milk yield and litter weight gain in rats. Proceedings of the Society for Experimental Biology and Medicine, 1967, 126, 41–45.
Laga, E. M., Driscoll, S. G., & Munro, H. N. Comparison of placentas from two socioeconomic groups: I. Morphometry. Pediatrics, 1972, 50, 24–33.
Leathwood, P. Influence of early undernutrition on behavioral development and learning in rodents. In G. Gottlieb (Ed.), Early influences. New York: Academic Press, 1978.
Lederman, S. A., & Rosso, P. Effects of food restriction on maternal weight and body composition in pregnant and non-pregnant rats. Growth, 1980, 44, 77–78.
Leon, M. Pheromonal mediation of maternal behavior. Advances in the Study of Behavior, 1977, 3, 177–196.
Leon, M., Croskerry, P. G., & Smith, G. K. Thermal control of mother-young contact in rats. Physiology and Behavior, 1978, 21, 793–811.
Levin, R., & Stern J. M. Maternal influences on the ontogeny of sucking and feeding rhythms in the rat. Journal of Comparative and Physiological Psychology, 1975, 89, 711–721.
Longo, L. D. Intrauterine growth retardation: A “mosaic” hypothesis of pathophysiology. Seminars in Perinatology, 1984, 8, 62–72.
Luckey, T. D., Mende, T. J., & Pleasants, J. The physical and chemical characterization of rat’s milk. Journal of Nutrition, 1954, 54, 345–349.
Lynch, A. Postnatal undernutrition: An alternative method. Developmental Psychobiology, 1976, 9, 39–48.
MacMillan, D. R. Secretion of the polypeptide hormones by the placentomaternal unit and their effects on the fetus and newborn. In Z. Laron & P. S. Tikva (Eds.), The influence of maternal hormones on the fetus and newborn. Basel: Karger, 1979.
Massaro, T. F., Levitsky, D. A., & Barnes, R. H. Protein malnutrition in the rat: Its effects on maternal behavior and pup development. Developmental Psychobiology, 1974, 7, 551–561.
Meschia, G., Battaglia, F. C., Hay, W. W., & Sparks, J. W. Utilization of substrates by the ovine placenta in vivo. Federation Proceedings, 1980, 39, 245–249.
Moltz, H., & Kilpatrick, S. J. Response to the maternal pheromone in the rat as protection against necrotizing enterocolitis. Neuroscience and Biobehavioral Reviews, 1980, 2, 277–280.
Morgane, P. J., Miller, M., Kemper, T., Stern, W., Forbes, W., Hall, R., Bronzino, J., Kissane, J., Hawrylewicz, E., & Resnick, O. The effects of protein malnutrition on the developing central nervous system in the rat. Neuroscience and Biobehavioral Reviews, 1978, 2 (3), 137–230.
Mueller, A. J., & Cox, W. M. Jr. The effect of changes in diet on the volume and composition of rat milk. Journal of Nutrition, 1946, 31, 249–259.
Munro, H. N., Pilistine, S. J., & Fant, M. E. The placenta in nutrition. Annual Review of Nutrition, 1983, 3, 97–124.
Murthy, L. S., Agarural, K. N., & Khanna, S. Placental morphometric and morphologic alterations in maternal undernutrition. American Journal of Obstetrics and Gynecology, 1976, 124, 641–645.
Myers, S. A., Sparks, J. W., Makowski, E. L., Meschia, G., & Battaglia, F. C. Relationship between placental blood flow and placental and fetal size in guinea pig. American Journal of Physiology, 1982, 243, H404–H409.
Orti, E. Steroid hormone formation and metabolism. In U. Stave (Ed.), Perinatal physiology. New York: Plenum Press, 1978.
Ota, K., & Yokoyama, A. Body weight and food consumption of lactating rats nursing various sizes of litters. Journal of Endocrinology, 1967, 38, 263–268.
Prieto, J. C., Cifuentes, I., & Serrano-Rios, M. hCS regulation during pregnancy. Obstetrics and Gynecology, 1976, 48, 297–301.
Ravelli, G-P., Stein, Z., & Süsser, M. Obesity in young men after famine exposure in utero and early infancy. New England Journal of Medicine, 1976, 295, 349–353.
Rosso, P. Maternal-fetal exchange during protein malnutrition in the rat: Placental transfer of alpha amino isobutyric acid. Journal of Nutrition, 1977, 107, 2002–2005. (a)
Rosso, P. Maternal-fetal exchange during protein malnutrition in the rat. Placental transfer of glucose and a non- metabolizable glucose analog. Journal of Nutrition, 1977, 107, 2006–2010. (b)
Rosso, P. Placental growth, development, and function in relation to maternal nutrition. Federation Proceedings, 1980, 39, 250–254.
Rosso, P., & Cramoy, C. Nutrition in pregnancy. In M. Winick (Ed.), Human nutrition: A comprehensive treatise, Vol. 1. New York: Plenum Press, 1979.
Rosso, P., & Kava, R. Effects of food restriction on cardiac output and blood flow to the uterus and placenta in the pregnant rat. Journal of Nutrition, 1980, 110, 2350–2354.
Rosso, P., & Streeter, M. R. Effects of food or protein restriction on plasma volume expansion in pregnant rats. Journal of Nutrition, 1979, 109, 1887–1892.
Rosso, P., Wasserman, M., Rozovski, S. J., & Velasco, E. Effects of maternal undernutrition on placental metabolism and function. In D. W. Young & J. M. Hicks (Eds.), The neonate. New York: Wiley, 1976.
Salas, M., & Torrero, C. Maternal behavior of rats undernourished in the early postnatal period. Boletin de Estudios Medicos y Biologicos Mexico, 1979, 30, 237–244.
Schreiner, R. L., Nolen, R. A., Borderman, P. W., Moorehead, H. C., Gresham, E. C., Lemons, J. A., & Escobedo, M. B. Fetal and maternal hormone response to starvation in the ewe. Pediatric Research, 1980, 14, 103–108.
Shah, A. K., Rajput, V. J., Bansil, K. K., & Kaul, K. K. Observation on some neonatal anthropometric and gestational characteristics in relation to placental morphology and histopathology. Indian Pediatrics, 1979, 16, 387–394.
Simmons, M. A., Meschia, G., Makowski, E. L., & Battaglia, F. C. Fetal metabolic response to maternal starvation. Pediatric Research, 1974, 8, 830–836.
Smart, J. L. Maternal behaviour of undernourished mother rats towards well fed and underfed young. Physiology and Behavior, 1976, 16, 147–149.
Smart, J. L., & Preece, J. Maternal behaviour of undernourished mother rats. Animal Behaviour, 1973, 21, 613–619.
Sparks, J. W., Hay, W. W., Jr., Meschia, G., & Battaglia, F. C. Partition of maternal nutrients to the placenta and fetus in the sheep. European Journal of Obstetrics, Gynecology and Reproductive Biology, 1983, 14, 331–340.
Spellacy, W. C., Buhi, W. C., Schram, J. D., Birk, S. A., & McCreary, S. A. Control of human chorionic somatomammotropin levels during pregnancy. Obstetrics and Gynecology, 1971, 37, 567–573.
Stephan, J. K., & Chow, B. F. Growth of progeny from rats underfed during gestation only. Federation Proceedings, 1968, 27, 728.
Surmaczynska, N. Z., Nitzan, M., Metzger, B. E., & Freinkel, N. Carbohydrate metabolism in pregnancy: XII. The effect of oral glucose on plasma concentrations of human placental lactogen and chorionic gonadotropin during late pregnancy in normal subjects and gestational diabetics. Israel Journal of Medical Science, 1974, 10, 1481–1486.
Thomson, A. M., Billewicz, W. Z., & Hytten, F. E. The weight of the placenta in relation to birthweight. The Journal of Obstetrics and Gynaecology of the British Commonwealth, 1969, 76, 865–872.
Widdowson, E. M., & McCance, R. A. The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proceedings of The Royal Society London, 1963, 158, 329–342.
Wiener, S. R., Fitzpatrick, R. M., Levin, R., Smotherman, W. P., & Levine, S. Alterations in the maternal behavior of rats rearing malnourished offspring. Developmental Psychobiology, 1977, 10, 243–254.
Wigglesworth, J. S. Experimental growth retardation in the fetal rat. Journal of Pathology and Bacteriology, 1964, 88, 1–21.
Wilkening, R. B., Anderson, S., Martensson, L., & Meschia, G. Relationship of transplacental diffusion to uterine blood flow. American Journal of Physiology, 1982, 242, H429–H436.
Winick, M. Fetal malnutrition and brain development. Journal of Pediatric Gastroenterology and Nutrition, 1983, 2 (Suppl. 1), 568–572.
Winick, M., & Noble, A. Cellular response during malnutrition at various ages. Journal of Nutrition, 1967, 91, 179–182.
Winick, M., Coscia, A., & Noble, A. Cellular growth of the human placenta: I. Normal placental growth. Pediatrics, 1967, 39, 248–263.
Yagil, R., Etzion, Z., & Berlyne, G. M. Changes in rat milk quantity and quality due to variations in litter size and high ambient temperature. Laboratory Animal Science, 1976, 26, 33–37.
Zamenhof, S., & Van Marthens, E. Nutritional influences on prenatal brain development. In G. Gottlieb (Ed.), Early influences. New York: Academic Press, 1978.
Zamenhof, S., van Marthens, E., & Grauel, L. DNA (cell number) and protein in neonatal rat brain: Alteration by timing of maternal dietary protein restriction. Journal of Nutrition, 1971, 9, 1265–1270.
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Jones, A.P., Crnic, L.S. (1986). Maternal Mediation of the Effects of Malnutrition. In: Riley, E.P., Vorhees, C.V. (eds) Handbook of Behavioral Teratology. Springer, Boston, MA. https://doi.org/10.1007/978-1-4613-2189-7_17
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