Hostname: page-component-cd9895bd7-gbm5v Total loading time: 0 Render date: 2024-12-28T00:39:31.409Z Has data issue: false hasContentIssue false
  • English
  • Français

Intergenerational effects of birth weight on glucose tolerance and reproductive performance

Published online by Cambridge University Press:  01 April 2009

A. M. Corson ,
J. Laws ,
J. C. Litten ,
I. J. Lean  and
L. Clarke
A. M. Corson
Affiliation:
Faculty of Natural Sciences, Imperial College London, Wye Campus, Wye, Kent TN25 5AH, UK
J. Laws
Affiliation:
Faculty of Natural Sciences, Imperial College London, Wye Campus, Wye, Kent TN25 5AH, UK
J. C. Litten
Affiliation:
Department of Agriculture, Policy and Development, The University of Reading, P.O. Box 237, Earley Gate, Reading, UK
I. J. Lean
Affiliation:
Faculty of Natural Sciences, Imperial College London, Wye Campus, Wye, Kent TN25 5AH, UK
L. Clarke*
Affiliation:
Faculty of Natural Sciences, Imperial College London, Wye Campus, Wye, Kent TN25 5AH, UK
*
E-mail: lynne.clark@imperial.ac.uk
Get access

Abstract

Women who were themselves small-for-gestational age (SGA) are at a greater risk of adulthood diseases such as non-insulin-dependent diabetes mellitus (NIDDM), and twice at risk of having an SGA baby themselves. The aim of this study was to examine the intergenerational pig. Low (L) and normal (N) birth weight female piglets were followed throughout their first pregnancy (generation 1 (G1)). After they had given birth, the growth and development of the lightest (l) and heaviest (n) female piglet from each litter were monitored until approximately 5 months of age (generation 2 (G2)). A glucose tolerance test (GTT) was conducted on G1 pig at ∼6 months of age and again during late pregnancy; a GTT was also conducted on G2 pigs at ∼4 months of age. G1 L offspring exhibited impaired glucose metabolism in later life compared to their G1 N sibling but in the next generation a similar scenario was only observed between l and n offspring born to G1 L mothers. Despite G1 L mothers showing greater glucose intolerance in late pregnancy and a decreased litter size, average piglet birth weight was reduced and there was also a large variation in litter weight; this suggests that they were, to some extent, prioritising their nutrient intake towards themselves rather than promoting their reproductive performance. There were numerous relationships between body shape at birth and glucose curve characteristics in later life, which can, to some extent, be used to predict neonatal outcome. In conclusion, intergenerational effects are partly seen in the pig. It is likely that some of the intergenerational influences may be masked due to the pig being a litter-bearing species.

Keywords

developmental programmingglucose tolerancelow birth weightporcine biomedical modelreproductive performance
Type
Full Paper
Information
animal , Volume 3 , Issue 4 , April 2009 , pp. 579 - 591
Copyright
Copyright © The Animal Consortium 2008

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Adams, PH 1971. Intra-uterine growth retardation in the pig. Biology of the Neonate 19, 341–353.CrossRefGoogle ScholarPubMed
Auldist, DE, Morrish, L, Eason, P, King, RH 1998. The influence of litter size on milk production of sows. Animal Science 67, 333–367.CrossRefGoogle Scholar
Barker, DJP 1994. The fetal origin of adult disease. Proceedings of the Royal Society, London 262, 37–43.Google Scholar
Barker, DJP 1998. In utero programming of chronic disease. Clinical Science 95, 115–128.CrossRefGoogle ScholarPubMed
Basak, UK, Pan, S 1994. Ethogram of porcine neonatal behaviour. Indian Journal of Animal Production and Management 10, 128–130.Google Scholar
Battaglia, FC, Meschia, G 1978. Principal substrates of fetal metabolism. Physiological Reviews 58, 499–527.CrossRefGoogle ScholarPubMed
Catalano, PM, Kirwan, JP, Haugel-De Mouzon, S, King, J 2003. Gestational diabetes and insulin resistance: role in short and long term implications for mother and fetus. The Journal of Nutrition 133, 1674S–1683S.CrossRefGoogle Scholar
Clarke, L, Firth, K, Heasman, L, Stephenson, T, Symonds, ME 2000. Influence of relative size at birth between female twin lambs on growth and glucose homeostasis during juvenile life. Reproduction Fertility and Development 12, 69–73.CrossRefGoogle ScholarPubMed
Collins, JW, Wu, SY, David, RJ 2002. Differing intergenerational birth weights among the descendants of US-born and foreign-born Whites and African Americans in Illinois. American Journal of Epidemiology 155, 210–216.CrossRefGoogle ScholarPubMed
Corson, AM, Laws, J, Laws, A, Litten, JC, Lean, IJ, Clarke, L 2008. Percentile growth charts for biomedical studies using a porcine model. Animal; doi:10.1017/S1751731108002966.CrossRefGoogle ScholarPubMed
DEFRA, 2003. Code of Recommendations for the Welfare of Livestock [online]. Retrieved February 14, 2005, from http://www.defra.gov.uk/animalh/welfare/farmed/pigs/pigcode.pdfGoogle Scholar
Drake, AJ, Walker, BR 2004. The intergenerational effects of fetal programming: non-genomic mechanisms for the inheritance of low birth weight and cardiovascular risk. The Journal of Endocrinology 180, 1–16.CrossRefGoogle ScholarPubMed
Drake, AJ, Smith, A, Betts, PR, Crowne, EC, Shield, JPH 2002. Type 2 diabetes in obese white children. Archives of Diseases in Childhood 86, 207–208.CrossRefGoogle ScholarPubMed
Dwyer, CM, Fletcher, JM, Stickland, NC 1993. Muscle cellularity and postnatal growth in the pig. Journal of Animal Science 71, 3339–3343.CrossRefGoogle ScholarPubMed
Elsley, FWH, Bathurst, EVJ, Bracewell, AG, Cunningham, JMM, Dent, JB, Dodsworth, TL, MacPherson, RM, Walker, N 1971. The effect of pattern of food intake in pregnancy upon sow productivity. Animal Production 13, 257–270.Google Scholar
Emanuel, I 1986. Maternal health during childhood and later reproductive performance. Annuals of New York Academic Science 477, 27–39.CrossRefGoogle ScholarPubMed
Emanuel, I, Albertman, HFE, Evans, SJW 1992. Intergenerational studies of human birthweight from the 1958 birth cohort. British Journal of Obstetrics and Gynaecology 99, 67–74.CrossRefGoogle ScholarPubMed
Fall, CHD 2001a. Non-industrialised countries and affluence. British Medical Bulletin 60, 33–50.CrossRefGoogle ScholarPubMed
Fall, CHD 2001b. The genesis of “Fetal origins of adult disease”. International Journal of Diabetes in Developing Countries 21, 3–11.Google Scholar
George, PB, England, DC, Siers, DG, Stanton, HC 1978. Diabetogenic effects of pregnancy in sows on plasma glucose and insulin release. Journal of Animal Science 46, 1694–1706.CrossRefGoogle ScholarPubMed
Girling, J, Dornhorst, A 2003. Pregnancy and diabetes mellitus. In Text book of Diabetes 2 (ed. J Pickup and G Williams), 3rd edition, pp. 65.1–65.39. Blackwell Science Ltd, Oxford.Google Scholar
Gluckman, PD, Hanson, MA, Pinal, C 2005. The developmental origins of adult disease. Maternal and Childhood Nutrition 1, 130–141.CrossRefGoogle ScholarPubMed
Guan, X, Matte, JJ, Ku, PK, Snow, JL, Burton, JL 2000. High chromium yeast supplementation improves glucose tolerance in pigs by decreasing hepatic extraction of insulin. The Journal of Nutrition 130, 1274–1279.CrossRefGoogle ScholarPubMed
Hackman, E, Emanuel, I, Belle, G, Daling, J 1983. Maternal birth weight and subsequent pregnancy outcome. Journal of American Medical Association 250, 2016–2019.CrossRefGoogle ScholarPubMed
Hales, CN, Barker, DJP 2001. The thrifty phenotype hypothesis. British Medical Journal 60, 5–20.Google ScholarPubMed
Hales, CN, Barker, DJP, Clark, PMS, Cox, LJ, Fall, C, Osmond, C, Winter, PD 1991. Fetal and infant growth and impaired glucose tolerance at age 64. British Medical Journal 303, 1019–1022.CrossRefGoogle ScholarPubMed
Hypponen, E, Smith, GD, Power, C 2003a. Effects of grandmothers, smoking in pregnancy on birth weight: intergenerational cohort study. British Medical Journal 327, 898.CrossRefGoogle ScholarPubMed
Hypponen, E, Smith, GD, Power, C 2003b. Effects of grandmothers, smoking in pregnancy on birth weight: intergenerational cohort study. British Medical Journal 327, 898.CrossRefGoogle ScholarPubMed
Kemp, B, Soede, NM, Vesseur, PC, Helmond, FA, Spoorenberg, JH, Frankena, K 1996. Glucose tolerance of pregnant sows is related to postnatal pig mortality. Journal of Animal Science 74, 879–885.CrossRefGoogle ScholarPubMed
King, RH 2000. Factors that influence milk production in well-fed sows. Journal of Animal Science 78, 19–25.CrossRefGoogle Scholar
Kingsbury DL 1992. Studies on the timing and the mechanism of boar induced first estrus in the pre-pubertal gilt, development, validation and application of a non surgical catherterization procedure. PhD, University of Saskatchewan, Saskatoon, Canada, pp. 57–61.Google Scholar
Klebanoff, MA, Graubard, BI, Kessel, SS, Berendes, HW 1984. Low birth weight across generations. Journal of American Medical Association 252, 2423–2427.CrossRefGoogle Scholar
Klebanoff, MA, Meirik, O, Berendes, HW 1989. Second-generation consequences of small-for-dates birth. Pediatrics 84, 343–347.CrossRefGoogle ScholarPubMed
Kyle, GC 1963. Diabetes and pregnancy. Annals of Internal Medicine 1, 1–9.Google Scholar
Leahy, JL 1990. Natural history of beta cell dysfunction in NIDDM. Diabetes Care 13, 952–1010.CrossRefGoogle ScholarPubMed
Lithell, HO, McKeigue, PM, Berglund, L, Mohsen, R, Litthell, U, Leon, DA 1996. Relation of size at birth to non-insulin dependent diabetes and insulin concentration in men aged 50–60 years. British Medical Journal 312, 406–410.CrossRefGoogle ScholarPubMed
Litten, JC, Mostyn, A, Perkins, KS, Corson, AM, Symonds, ME, Clarke, L 2005. Effect of administration of recombinant human leptin during the neonatal period on the plasma concentration and gene expression of leptin in the piglet. Biology of the Neonate 87, 1–7.CrossRefGoogle ScholarPubMed
Little, RE 1987. Mother’s and father’s birth weight as predictors of infant birth weight. Pediatrics Perinatal Epidemiology 1, 19–31.CrossRefGoogle Scholar
Lumey, LH 1998. Reproductive outcomes in women prenatally exposed to undernutrition: a review of findings from the Dutch Famine Birth Cohort. The Proceedings of the Nutrition Society 57, 129–135.CrossRefGoogle ScholarPubMed
McCance, DR 1994. Birth weight and non-insulin dependent diabetes: thrifty genotype, thrifty phenotype, or surviving small baby genotype. British Medical Journal 308, 942–945.CrossRefGoogle ScholarPubMed
McCarron, P, Smith, GD, Hattersley, AT 2004. Type 2 diabetes in grandparents and birth weight in offspring and grandchildren in the ALSPAC study. Journal of Epidemiology and Community Health 58, 517–522.CrossRefGoogle ScholarPubMed
Mostyn, A, Litten, JC, Perkins, KS, Euden, PJ, Corson, AM, Symonds, ME, Clarke, L 2005. Influence of size at birth on the endocrine profiles and expression of uncoupling proteins in subcutaneous adipose tissue, lung, and muscle of neonatal pigs. America Journal of Physiology-Regulatory, I 288, R1536–R1542.Google ScholarPubMed
Mussey, RD 1949. Nutrition and human reproduction: an historical review. American Journal of Obstetrics and Gynecology 57, 1037–1048.CrossRefGoogle ScholarPubMed
Naeye, RL 1983. Maternal age, obstetric complications, and the outcome of pregnancy. Obstetrics and Gynecology 61, 210–216.Google ScholarPubMed
Ong, KKL, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB 2000. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. British Medical Journal 320, 967–971.CrossRefGoogle ScholarPubMed
Ounsted, M, Ounsted, C 1966. Maternal regulation of intrauterine growth. Nature, London 212, 995–997.CrossRefGoogle Scholar
Ozanne, SE, Hales, CN 1999. The long-term consequences of intrauterine protein malnutrition for glucose metabolism. The Proceedings of the Nutrition Society 58, 615–619.CrossRefGoogle ScholarPubMed
Phillips, DIW 1996. Insulin resistance as a programmed response to fetal undernutrition. Diabetologia 39, 1119–1122.CrossRefGoogle ScholarPubMed
Phillips, DIW 1998. Birth weight and the future development of diabetes. Diabetes Care 21, B150–B155.Google ScholarPubMed
Phillips, DIW, Barker, DJP, Hales, CN, Hirst, S, Osmond, C 1994. Thinness at birth and insulin resistance in adult life. Diabetologia 37, 150–154.CrossRefGoogle ScholarPubMed
Phipps, K, Barker, DJP, Hales, CN, Fall, CHD, Osmond, C, Clark, PMS 1993. Fetal growth and impaired glucose tolerance in men and women. Diabetologia 36, 225–228.CrossRefGoogle ScholarPubMed
Pond, WG, Mersmann, HJ 2001. General characteristics. In Biology of the domestic pig, pp. 15–20. Cornell University Press, USA.Google Scholar
Poore, KR, Fowden, AL 2002. The effect of birth weight on glucose tolerance in pigs at 3 and 12 months of age. Diabetologia 45, 1247–1254.CrossRefGoogle ScholarPubMed
Poore, KR, Fowden, AL 2003. Insulin sensitivity in juvenile and adult large white pigs of low and high birth weight. Diabetologia 47, 340–348.CrossRefGoogle Scholar
Powell, SE, Aberle, ED 1980. Effects of birth weight on growth and carcass composition of swine. Journal of Animal Science 50, 860–868.CrossRefGoogle ScholarPubMed
Rosillon-Warnier, A, Paquay, R 1984. Development and consequences of teat-order in piglets. Applied Animal Behavior Science 13, 47–58.CrossRefGoogle Scholar
Rydhmer, L, Eliasson, L, Stern, S, Anderson, K, Einarsson, S 1989. Effects of piglet weight and fraternity size on performance puberty and farrowing results. Acta Agriculture Scandinavia 39, 397–406.CrossRefGoogle Scholar
Skjaerven, R, Wilcox, AJ, Oyen, N, Magnus, P 1997. Mothers’ birth weight and survival of their offspring: population based study. British Medical Journal 314, 1376–1380.CrossRefGoogle ScholarPubMed
Stein, AD, Lumey, LH 2000. The relationship between maternal and offspring birth weights after maternal prenatal famine exposure: The Dutch Famine Birth Cohort Study. Human Biology 72, 641–654.Google ScholarPubMed
Stewart, RJC, Sheppard, H, Preece, R, Waterlow, JC 1980. The effect of rehabilitation at different stages of development of rats marginally malnourished for ten to twelve generations. The British Journal of Nutrition 43, 403–412.CrossRefGoogle ScholarPubMed
Wallace, J, Bourke, D, Da Silva, P, Aitken, R 2001. Nutrient partitioning during adolescent pregnancy. Reproduction 122, 347–357.CrossRefGoogle ScholarPubMed
Walton, A, Hammond, J 1938. The maternal effects on growth and conformation in Shire horse-Shetland pony crosses. Proceedings of the Royal Society, London 125, 311–335.Google Scholar
Weekes, TEC 1986. Insulin and growth. In Control and manipulation of animal growth. Butterworths, London.Google Scholar