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Placental restriction in multi-fetal pregnancies and between-twin differences in size at birth alter neonatal feeding behaviour in the sheep

Published online by Cambridge University Press:  06 April 2017

R. F. Peter ,
J. Gugusheff ,
A. L. Wooldridge Open the ORCID record for A. L. Wooldridge [Opens in a new window] ,
K. L. Gatford Open the ORCID record for K. L. Gatford [Opens in a new window]  and
B. S. Muhlhausler
R. F. Peter
Affiliation:
Department of Food and Wine Science, School of Agriculture, Food and Wine, FOODplus Research Centre, The University of Adelaide, Adelaide, SA, Australia
J. Gugusheff
Affiliation:
Department of Food and Wine Science, School of Agriculture, Food and Wine, FOODplus Research Centre, The University of Adelaide, Adelaide, SA, Australia
A. L. Wooldridge
Affiliation:
Discipline of Obstetrics and Gynaecology, Adelaide Medical School, Adelaide, SA, Australia Robinson Research Institute, The University of Adelaide, Adelaide, SA, Australia
K. L. Gatford
Affiliation:
Discipline of Obstetrics and Gynaecology, Adelaide Medical School, Adelaide, SA, Australia Robinson Research Institute, The University of Adelaide, Adelaide, SA, Australia
B. S. Muhlhausler*
Affiliation:
Department of Food and Wine Science, School of Agriculture, Food and Wine, FOODplus Research Centre, The University of Adelaide, Adelaide, SA, Australia
*
*Address for correspondence: B. S. Muhlhausler, FOODplus Research Centre, The University of Adelaide, Adelaide, South Australia 5064, Australia. (Email beverly.muhlhausler@adelaide.edu.au)
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Abstract

Most individuals whose growth was restricted before birth undergo accelerated or catch-up neonatal growth. This is an independent risk factor for later metabolic disease, but the underlying mechanisms are poorly understood. This study aimed to test the hypothesis that natural and experimentally induced in utero growth restriction increase neonatal appetite and milk intake. Control (CON) and placentally restricted (PR) ewes carrying multiple fetuses delivered naturally at term. Outcomes were compared between CON (n=14) and PR (n=12) progeny and within twin lamb pairs. Lamb milk intake and feeding behaviour and ewe milk composition were determined using a modified weigh-suckle-weigh procedure on days 15 and 23. PR lambs tended to have lower birth weights than CON (−15%, P=0.052). Neonatal growth rates were similar in CON and PR, whilst heavier twins grew faster in absolute but not fractional terms than their co-twins. At day 23, milk protein content was higher in PR than CON ewes (P=0.038). At day 15, PR lambs had fewer suckling bouts than CON lambs and in females light twins had more suckling attempts than their heavier co-twins. Birth weight differences between twins positively predicted differences in milk intakes. Lactational constraint and natural prenatal growth restriction in twins may explain the similar milk intakes in CON and PR. Within twin comparisons support the hypothesis that prenatal constraint increases lamb appetite, although this did not increase milk intake. We suggest that future mechanistic studies of catch-up growth be performed in singletons and be powered to assess effects in each sex.

Keywords

catch-up growthfetal growth restrictionmilk compositionmilk intakenewborn
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 8 , Issue 3 , June 2017 , pp. 357 - 369
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Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2017 

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Footnotes

†

Joint senior authors.

References

1. Rosenberg, A. The IUGR newborn. Semin Perinatol. 2008; 32, 219–224.Google Scholar
2. Sharma, D, Shastri, S, Farahbakhsh, N, Sharma, P. Intrauterine growth restriction – Part 1. J Matern Fetal Neonatal Med. 2016; 29, 3977–3987.Google Scholar
3. Sankaran, S, Kyle, PM. Aetiology and pathogenesis of IUGR. Best Pract Res Clin Obstet Gynaecol. 2009; 23, 765–777.Google Scholar
4. Tenovuo, A, Kero, P, Piekkala, P, et al. Growth of 519 small for gestational age infants during the first two years of life. Acta Paed Scand. 1987; 76, 636–646.CrossRefGoogle ScholarPubMed
5. Albertsson-Wikland, K, Karlberg, J. Postnatal growth of children born small for gestational age. Acta Paediatrica. 1997; 423, 193–195.Google Scholar
6. Eriksson, JG, Forsen, T, Tuomilehto, J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. BMJ. 1999; 318, 427–431.Google Scholar
7. Forsen, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176–182.Google Scholar
8. Huxley, RR, Shiell, AW, Law, CM. The role of size at birth and postnatal catch-up growth in determining systolic blood pressure: a systematic review of the literature. J Hypertens. 2000; 18, 815–831.Google Scholar
9. Ong, KK, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. BMJ. 2000; 320, 967–971.CrossRefGoogle ScholarPubMed
10. Ounsted, M, Sleigh, G. The infant’s self-regulation of food intake and weight gain. Difference in metabolic balance after growth constraint or acceleration in utero. Lancet. 1975; 1, 1393–1397.CrossRefGoogle ScholarPubMed
11. Greenwood, PL, Hunt, AS, Hermanson, JW, Bell, AW. Effects of birth weight and postnatal nutrition on neonatal sheep: I. Body growth and composition, and some aspects of energetic efficiency. J Anim Sci. 1998; 76, 2354–2367.Google Scholar
12. Vickers, MH, Breier, BH, Cutfield, WS, Hofman, PL, Gluckman, PD. Fetal origins of hyperphagia, obesity, and hypertension and postnatal amplification by hypercaloric nutrition. Am J Physiol. 2000; 279, E83–E87.Google Scholar
13. Laporte-Broux, B, Roussel, S, Ponter, AA, et al. Long-term consequences of feed restriction during late pregnancy in goats on feeding behavior and emotional reactivity of female offspring. Physiol Behav. 2012; 106, 178–184.Google Scholar
14. Laporte-Broux, B, Roussel, S, Ponter, AA, et al. Short-term effects of maternal feed restriction during pregnancy on goat kid morphology, metabolism, and behavior. J Anim Sci. 2011; 89, 2154–2163.Google Scholar
15. Alexander, G. Studies on the placenta of the sheep. J Reprod Fertil. 1964; 7, 289–305.Google Scholar
16. Robinson, JS, Kingston, EJ, Jones, CT, Thorburn, GD. Studies on experimental growth retardation in sheep. The effect of removal of endometrial caruncles on fetal size and metabolism. J Develop Physiol. 1979; 1, 379–398.Google Scholar
17. De Blasio, MJ, Gatford, KL, McMillen, IC, Robinson, JS, Owens, JA. Placental restriction of fetal growth increases insulin action, growth and adiposity in the young lamb. Endocrinology. 2006; 148, 1350–1358.Google Scholar
18. De Blasio, MJ, Gatford, KL, Robinson, JS, Owens, JA. Placental restriction of fetal growth reduces size at birth and alters postnatal growth, feeding activity, and adiposity in the young lamb. Am J Physiol Regul Integr Comp Physiol. 2007; 292, R875–R886.Google Scholar
19. O’Dowd, R, Kent, JC, Moseley, JM, Wlodek, ME. Effects of uteroplacental insufficiency and reducing litter size on maternal mammary function and postnatal offspring growth. Am J Physiol Regul Integr Comp Physiol. 2008; 294, R539–R548.Google Scholar
20. National Health and Medical Research Council. Australian Code for the Care and Use of Animals for Scientific Purposes, 8th edn, 2013. National Health and Medical Research Council: Canberra.Google Scholar
21. Kaur, M, Wooldridge, AL, Wilkes, MJ, et al. Placental restriction in multi-fetal pregnancies increases spontaneous ambulatory activity during daylight hours in young adult female sheep. J Dev Orig Health Dis. 2016; 7, 525–537.Google Scholar
22. Vonnahme, KA, Arndt, WJ, Johnson, ML, Borowicz, PP, Reynolds, LP. Effect of morphology on placentome size, vascularity, and vasoreactivity in late pregnant sheep. Biol Reprod. 2008; 79, 976–982.Google Scholar
23. Muhlhausler, BS, Adam, CL, Findlay, PA, Duffield, JA, McMillen, IC. Increased maternal nutrition alters development of the appetite-regulating network in the brain. FASEB J. 2006; 20, 1257–1259.Google Scholar
24. Hinch, GN. The suckling behaviour of triplet, twin and single lambs at pasture. Appl Anim Behav Sci. 1989; 22, 39–48.Google Scholar
25. Nommsen, LA, Lovelady, CA, Heinig, MJ, Lonnerdal, B, Dewey, KG. Determinants of energy, protein, lipid, and lactose concentrations in human milk during the first 12 mo of lactation: the DARLING Study. Am J Clin Nutr. 1991; 53, 457–465.Google Scholar
26. Falconer, J, Owens, JA, Allotta, E, Robinson, JS. Effect of restriction of placental growth on the concentrations of insulin, glucose and placental lactogen in the plasma of sheep. J Endocrinol. 1985; 106, 7–11.Google Scholar
27. Hayden, TJ, Thomas, CR, Forsyth, IA. Effect of number of young born (litter size) on milk yield of goats: role for placental lactogen. J Dairy Sci. 1979; 62, 53–63.Google Scholar
28. Martal, J, Djiane, J. Mammotrophic and growth promoting activities of a placental hormone in sheep. J Steroid Biochem. 1977; 8, 415–417.Google Scholar
29. Leibovich, H, Gertler, A, Bazer, F, Gootwine, E. Effects of recombinant ovine placental lactogen and recombinant ovine growth hormone on growth of lambs and milk production of ewes. Livestock Production Sci. 2001; 68, 79–86.Google Scholar
30. Prentice, P, Ong, KK, Schoemaker, MH, et al. Breast milk nutrient content and infancy growth. Acta Paediatr. 2016; 105, 641–647.Google Scholar
31. Koletzko, B, von Kries, R, Closa, R, et al. Lower protein in infant formula is associated with lower weight up to age 2 y: a randomized clinical trial. Am J Clin Nutr. 2009; 89, 1836–1845.Google Scholar
32. Torres-Hernandez, G, Hohenboken, W. Relationships between ewe milk production and composition and preweaning lamb weight gain. J Anim Sci. 1980; 50, 597–603.Google Scholar
33. Domany, KA, Mandel, D, Hausman Kedem, M, Lubetzky, R. Breast milk fat content of mothers to small-for-gestational-age infants. J Perinatol. 2015; 35, 444–446.Google Scholar
34. Bobinski, R, Mikulska, M, Mojska, H, Simon, M. Comparison of the fatty acid composition of transitional and mature milk of mothers who delivered healthy full-term babies, preterm babies and full-term small for gestational age infants. Eur J Clin Nutr. 2013; 67, 966–971.Google Scholar
35. Daly, SE, Di Rosso, A, Owens, RA, Hartmann, PE. Degree of breast emptying explains changes in the fat content, but not fatty acid composition, of human milk. Exp Physiol. 1993; 78, 741–755.Google Scholar
36. Jaquiery, AL, Oliver, MH, Bloomfield, FH, Harding, JE. Periconceptional events perturb postnatal growth regulation in sheep. Pediatr Res. 2011; 70, 261–266.Google Scholar
37. Cameron, EZ. Is suckling behaviour a useful predictor of milk intake? A review. Animal Behaviour. 1998; 56, 521–532.CrossRefGoogle ScholarPubMed
38. van der Linden, DS, Sciascia, Q, Sales, F, McCoard, SA. Placental nutrient transport is affected by pregnancy rank in sheep. J Anim Sci. 2013; 91, 644–653.Google Scholar
39. Muhlhausler, BS, Hancock, SN, Bloomfield, FH, Harding, R. Are twins growth restricted? Pediatr Res. 2011; 70, 117–122.Google Scholar
40. Hancock, SN, Oliver, MH, McLean, C, Jaquiery, AL, Bloomfield, FH. Size at birth and adult fat mass in twin sheep are determined in early gestation. J Physiol. 2012; 590, 1273–1285.Google Scholar
41. Davies, MJ. Fetal programming: the perspective of single and twin pregnancies. Reprod Fertil Dev. 2005; 17, 379–386.Google Scholar
42. Morrison, JL. Sheep models of intrauterine growth restriction: fetal adaptations and consequences. Clin Exp Pharmacol Physiol. 2008; 35, 730–743.Google Scholar
43. Benson, ME, Henry, MJ, Cardellino, RA. Comparison of weigh-suckle-weigh and machine milking for measuring ewe milk production. J Anim Sci. 1999; 77, 2330–2335.Google Scholar
44. Muhlhausler, BS, Duffield, JA, Ozanne, SE, et al. The transition from fetal growth restriction to accelerated postnatal growth: a potential role for insulin signalling in skeletal muscle. J Physiol. 2009; 587, 4199–4211.Google Scholar
45. Gruenwald, P. Growth of the human fetus. II. Abnormal growth in twins and infants of mothers with diabetes, hypertension, or isoimmunization. Am J Obstet Gynecol. 1966; 94, 1120–1132.Google Scholar
46. Thompson, GE. The intake of milk by suckled, newborn lambs and the effects of twinning and cold exposure. Br J Nutr. 1983; 50.Google Scholar
47. Dove, H. Estimation of the intake of milk by lambs, from the turnover of deuterium- or tritium-labelled water. Br J Nutr. 1988; 60, 375–387.CrossRefGoogle ScholarPubMed