Hostname: page-component-8448b6f56d-qsmjn Total loading time: 0 Render date: 2024-04-18T12:24:05.189Z Has data issue: false hasContentIssue false

Organ-selective growth in the offspring of protein-restricted mothers

Published online by Cambridge University Press:  09 March 2007

Mina Desai
Affiliation:
Department of Clinical Biochemistry, University of Cambridge, Addenbrooke's Hospital, Hills Road, CambridgeCB2 2QR
Nigel J. Crowther
Affiliation:
Department of Clinical Biochemistry, University of Cambridge, Addenbrooke's Hospital, Hills Road, CambridgeCB2 2QR
Alan Lucas
Affiliation:
Dunn Nutritional Unit, University of Cambridge and Medical Research Council, Downhams Lane, Milton Road, CambridgeCB4 1XJ
C. Nicholas Hales
Affiliation:
Department of Clinical Biochemistry, University of Cambridge, Addenbrooke's Hospital, Hills Road, CambridgeCB2 2QR
Rights & Permissions [Opens in a new window]

Abstract

Core share and HTML view are not available for this content. However, as you have access to this content, a full PDF is available via the ‘Save PDF’ action button.

Recent epidemiological studies in people whose birth weights were recorded many years ago suggest links between impaired growth during early life and the development of diseases, including diabetes, much later in life. The long-term effects of retarded early growth are proposed to result from malnutrition at critical periods of fetal or infant development leading to reduction in the growth of organs and permanent changes in their metabolism or structure, or both. In order to investigate this, a rat model was established which involved feeding either a diet containing 200 g protein/kg or an isoenergetic diet containing 80 g protein/kg to pregnant and lactating rats. In addition, cross-fostering techniques were employed which allowed a separate evaluation of the prenatal or the postnatal periods. The offspring were studied at 21 d of age or were weaned onto a normal laboratory chow and studied at 11 months of age. The 80g protein/kg diet during pregnancy did not affect the overall reproductive performance although more subtle differences were evident. Permanent growth retardation was evident in offspring subjected to maternal protein restriction during the postnatal period. At 21 d of age the offspring of protein-restricted mothers exhibited selective changes in organ growth: compared with the body weight, the lung and brain experienced a smaller decrease in weight; the heart, kidney and thymus decreased proportionately; whereas, the pancreas, spleen, muscle and liver showed a greater reduction in weight. In older animals the muscle weight was lower in the male rats and the relative weight ofpancreas was increased in the female rats.

Type
General Nutrition
Copyright
Copyright © The Nutrition Society 1996

References

REFERENCES

Allen, L. H. & Zeman, F. J. (1973). Kidney function in the progeny of protein-deficient rats. Journal of Nurrition 103, 14671478.Google ScholarPubMed
Barker, D. J. P., Bull, A. R., Osmond, C. & Simmonds, S. J. (1990). Fetal and placental size and risk of hypertension in adult life. Britsh Medical Journal 301, 259262.CrossRefGoogle ScholarPubMed
Barker, D. J. P., Hales, C. N., Fall, C. H. D., Osmond, C., Phipps, K. & Clark, P. M. S. (1993). Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia 36, 6267.CrossRefGoogle ScholarPubMed
Barker, D. J. P., Meade, T. W., Fall, C. H. D., Lee, A., Osmond, C., Phipps, K. & Stirling, Y. (1992). Relation of fetal and infant growth to plasma fibrinogen and factor VII concentrations in adult life. British Medical Journal 304, 148152.CrossRefGoogle ScholarPubMed
Bedi, K. S., Birzgalis, A. R., Mahon, M., Smart, J. L. & Wareham, A. C. (1982). Early life undernutrition in rats. British Journal of Nutrition 47, 417430.CrossRefGoogle ScholarPubMed
Cahill, G. F.(1970). Starvation in man. New England Journal of Medicine 282, 668675.Google ScholarPubMed
DeFronzo, R. A. (1988). The triumvirate: beta cell, muscle, liver. A collusion responsible for NIDDM. Diabetes 37, 667687.CrossRefGoogle ScholarPubMed
Desai, M., Crowther, N., Lucas, A. & Hales, C. N. (1994). Programming of hepatic metabolismby early protein restriction. Diabetalogia 37, Suppl.1, A71, Abstr.Google Scholar
Desai, M., Crowther, N. J., Ozanne, S. E., Lucas, A. & Hales, C. N. (1995). Adult glucose and lipid metabolism may be programmed during fetal life. Biochemical Society Transactions 23, 329333.CrossRefGoogle ScholarPubMed
Fleagle, J. G., Samonds, K. W. & Hegsted, D. M. (1975). Physical growth of cebus monkeys, cebus albifrons during protien or calorie deficiency. American Journal of Clinical Nutrition, 28, 246253.CrossRefGoogle ScholarPubMed
Garrow, J. S., Fletcher, K. & Halliday, D. (1965). Body composition in severe infantile malnutrition. Journal of Clinical Investigation 44, 417425.CrossRefGoogle ScholarPubMed
Gruenwald, P. (1963). Chronic fetal distress and placental insufficiency. Biology of the Neonate 5, 215219.CrossRefGoogle ScholarPubMed
Hales, C. N. & Barker, D. J. P. (1992). Type 2 (non-insulin-dependent) diabetes mellitus: thethrifty phenotype hypothesis. Diabetologia 35, 595601.CrossRefGoogle ScholarPubMed
Hales, C. N., Barker, D. J. P., Clark, P. M. S., Cox, L. J., Fall, C., Osmond, C. & Winter, P. D. (1991). Fetal and infant growth and impaired glucose tolerance at age 64 years. British Medical Journal 303, 10191022.CrossRefGoogle Scholar
Haltia, M., Berlin, O., Schucht, H. & Sourander, P. (1978). Postnatal differentiation and growth of skeletal muscle fibres in normal and undernourished rats. Journal of Neurology Sciences 36, 2539.CrossRefGoogle ScholarPubMed
Hinchcliffe, S. A., Lynch, M. R. J., Sargent, P. H., Howard, C. V. & Van Velzen, D. (1992). The effect of intrauterine growth retardation on the development of renal nephrons. British Journal of Obstetrics and Gynaecology 99, 296301.CrossRefGoogle Scholar
Howells, K. F. & Jordon, T. C. (1978). The effects of pre- and perinatal undernutrition on the succinic dehydrogenase content of muscle fibres from fast and slow rat muscles. Histochemistry 58, 97102.CrossRefGoogle ScholarPubMed
James, W. P. T. & Coore, H. G. (1970). Persistent impairment of insulin secretion and glucose tolerance after malnutrition. American Journal of Clinical Nutrition 23, 386389.CrossRefGoogle ScholarPubMed
McCance, R. A. & Widdowson, E. M. (1966). Protein deficiencies and calorie deficiencies. Lancet ii, 158159.CrossRefGoogle Scholar
McCance, R. A. & Widdowson, E. M. (1974). The determinants of growth and form. Proceedings of the Royal Society of London 185, 117.Google ScholarPubMed
Milner, R. D. G. (1971). Metabolic and hormonal responses to glucose and glucagon in patients with infantile malnutrition. Pediatric Research 5, 3339.CrossRefGoogle Scholar
Ogata, E. S., Bussey, M., LaBarbera, A. & Finley, S. (1985). Altered growth, hypoglycemia, hypoalaninemia, and ketonemia in the young rat: postnatal consequences of intrauterine growth retardation. Pediatric Research 19, 3237.CrossRefGoogle Scholar
Phillips, D. I. W., Barker, D. J. P., Hales, C. N., Hirst, S. & Osmond, C. (1994). Thinness at birth and insulin resistance in adult life. Diabetologia 37, 150154.CrossRefGoogle ScholarPubMed
Pimstone, B. L. (1976). Endocrine function in protein-calorie malnutrition. Clinical Endocrinology 5, 7995.Google ScholarPubMed
Rider, A. A. & Simonson, M. (1974). The relationship between maternal diet, birthweight and behaviour of the offspring in the rat. Nutrition Reports International 10, 1922.Google Scholar
Robinson, S. M., Wheeler, T., Hayes, M. C., Barker, D. J. P. & Osmond, C. (1991). Fetal heart rate and intrauterine growth. British Journal of Obstetrics and Gynaecology 98, 12231227.CrossRefGoogle ScholarPubMed
Ross, P. (1975). Maternal malnutrition and placental transfer of α-aminoisobutyric acid in the rat. Science 187, 648649.CrossRefGoogle Scholar
Sampson, D. A., Hunsaker, H. A. & Jansen, G. R. (1986). Dietary protein quality, protein quantity and food intake: effects on lactation and on protein synthesis and tissue composition in mammary tissue and liver in rats. Journal of Nutrition 116, 365375.CrossRefGoogle ScholarPubMed
Simmons, R. A., Gounis, A. S., Bangalore, S. A. & Ogata, E. S. (1992). Intrauterine growth retardation: fetal glucose transport is diminished in lung but spared in brain. Pediurric Research 31, 5963.CrossRefGoogle ScholarPubMed
Smart, J. L. (1993). Behavioural consequences of undernutrition. Proceedings ofthe Nutrition Society 52, 189199.CrossRefGoogle Scholar
Snoeck, A., Remacle, C., Reusens, B. & Hoet, J. J. (1990). Effect of a low protein diet during pregnancy on the fetal rat endocrine pancreas. Biology of the Neonatae 57, 107118.CrossRefGoogle ScholarPubMed
Stewart, R. J. C., Preece, R. F. & Sheppard, H. G. (1975). Twelve generations of marginal protein deficiency. British Journal of Nutrition 33, 233253.CrossRefGoogle ScholarPubMed
Swenne, I., Crace, C. J. & Milner, R. D. G. (1987). Persistent impairment of insulin secretory response to glucose in adult rats after limited periods of prolein-calorie malnutrition in early life. Diabetes 36, 454458.CrossRefGoogle Scholar
Weinkove, C., Weinkove, E. A. & Pimstone, B. L. (1974). Insulin release and pancreatic islet volume in malnourished rats. South African Medical Journal 48, 1888.Google Scholar
Widdowson, E. M. (1971). Intra-uterine growth retardation in the pig. 1. Organ size and cellular development at birth and after growth to maturity. Biology of the Neonate, 19, 329340.CrossRefGoogle Scholar
Widdowson, E. M. & McCance, R. A. (1960). Some effects of accelerating growth. 1. General somatic development. Proceedings of the Royal Society London 152, 188206.Google Scholar
Widdowson, E. M. & McCance, R. A. (1975). A Review: new thoughts on growth. Pediatric Research 9, 154156.CrossRefGoogle ScholarPubMed
Winick, M. (1971). Cellular changes during placental and fetal growth. American Journal of Obstetrics and Gynecology 109, 166176.CrossRefGoogle ScholarPubMed
Winick, M. & Noble, A. (1966). Cellular response in rats during malnutrition at various ages. Journal of Nutrition 89, 300306.CrossRefGoogle ScholarPubMed
Winick, M., Rosso, P. & Waterlow, J. C. (1970). Cellular growth of cerebrum, cerebellum and brain stem in normal and marasmic children. Experimental Neurology 26, 393400.CrossRefGoogle ScholarPubMed
Wunderlich, S. M., Baliga, B. S. & Munro, H. N. (1979). Rat placental protein synthesis and peptide hormone secretion in relation to malnutrition from protein deficiency and alcohol administration. Journal of Nutrition 109, 15341541.CrossRefGoogle ScholarPubMed
Young, M. & Widdowson, E. M. (1975). The influence of diets deficient in energy, or in protein, on conceptus weight, and the placental transfer of a non-metabolisable amino acid in the guinea pig. Biology ofthe Neonate 27, 184191.CrossRefGoogle ScholarPubMed