Hostname: page-component-76fb5796d-vvkck Total loading time: 0 Render date: 2024-04-26T16:13:14.144Z Has data issue: false hasContentIssue false

Placental restriction in multi-fetal pregnancies increases spontaneous ambulatory activity during daylight hours in young adult female sheep

Published online by Cambridge University Press:  23 June 2016

M. Kaur
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia Discipline of Obstetrics & Gynaecology, School of Medicine, The University of Adelaide, SA, Australia
A. L. Wooldridge
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia Discipline of Obstetrics & Gynaecology, School of Medicine, The University of Adelaide, SA, Australia
M. J. Wilkes
Affiliation:
School of Animal and Veterinary Sciences, The University of Adelaide, SA, Australia
W. S. Pitchford
Affiliation:
School of Animal and Veterinary Sciences, The University of Adelaide, SA, Australia
P. I. Hynd
Affiliation:
School of Animal and Veterinary Sciences, The University of Adelaide, SA, Australia
G. K. McConell
Affiliation:
Institute of Sport, Exercise and Active Living, Victoria University, Melbourne, VIC, Australia
K. L. Gatford*
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia Discipline of Obstetrics & Gynaecology, School of Medicine, The University of Adelaide, SA, Australia
*
*Address for correspondence: Dr K. L. Gatford, Discipline of Obstetrics & Gynaecology, School of Medicine, University of Adelaide, SA 5005, Australia. (Email Kathy.gatford@adelaide.edu.au)

Abstract

Intrauterine growth restriction (IUGR) has adverse effects on metabolic health and early life, whereas physical activity is protective against later development of metabolic disease. Relationships between birth weight and physical activity in humans, and effects of IUGR on voluntary activity in rodents, are mixed and few studies have measured physical activity in a free-ranging environment. We hypothesized that induced restriction of placental growth and function (PR) in sheep would decrease spontaneous ambulatory activity (SAA) in free-ranging adolescent and young adult progeny from multi-fetal pregnancies. To test this hypothesis, we used Global Positioning System watches to continuously record SAA between 1800 and 1200 h the following day, twice during a 16-day recording period, in progeny of control (CON, n=5 males, 9 females) and PR pregnancies (n=9 males, 10 females) as adolescents (30 weeks) and as young adults (43 weeks). PR reduced size at birth overall, but not in survivors included in SAA studies. In adolescents, SAA did not differ between treatments and females were more active than males overall and during the day (each P<0.001). In adults, daytime SAA was greater in PR than CON females (P=0.020), with a similar trend in males (P=0.053) and was greater in females than males (P=0.016). Adult SAA was negatively correlated with birth weight in females only. Contrary to our hypothesis, restricted placental function and small size at birth did not reduce progeny SAA. The mechanisms for increased daytime SAA in adult female PR and low birth weight sheep require further investigation.

Type
Original Article
Copyright
© Cambridge University Press and the International Society for Developmental Origins of Health and Disease 2016 

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

1. Ergaz, Z, Avgil, M, Ornoy, A. Intrauterine growth restriction-etiology and consequences: what do we know about the human situation and experimental animal models? Reprod Toxicol. 2005; 20, 301322.CrossRefGoogle ScholarPubMed
2. Robinson, JS, Moore, VM, Owens, JA, McMillen, IC. Origins of fetal growth restriction. Eur J Obstet Gynecol Reprod Biol. 2000; 92, 1319.CrossRefGoogle ScholarPubMed
3. Henriksen, T, Clausen, T. The fetal origins hypothesis: placental insufficiency and inheritance versus maternal malnutrition in well-nourished populations. Acta Obstet Gynecol Scand. 2002; 81, 112114.CrossRefGoogle ScholarPubMed
4. Kramer, MS. The epidemiology of adverse pregnancy outcomes: an overview. J Nutr. 2003; 133(Suppl. 2), 1592S1596S.CrossRefGoogle ScholarPubMed
5. Gagnon, R. Placental insufficiency and its consequences. Eur J Obstet Gynecol Reprod Biol. 2003; 110(Suppl. 1), S99107.CrossRefGoogle ScholarPubMed
6. Sankaran, S, Kyle, PM. Aetiology and pathogenesis of IUGR. Best Pract Res Clin Obstet Gynaecol. 2009; 23, 765777.CrossRefGoogle ScholarPubMed
7. Clayton, PE, Cianfarani, S, Czernichow, P, et al. Management of the child born small for gestational age through to adulthood: a consensus statement of the International Societies of Pediatric Endocrinology and the Growth Hormone Research Society. J Clin Endocrinol Metab. 2007; 92, 804810.CrossRefGoogle ScholarPubMed
8. Andersen, LG, Angquist, L, Gamborg, M, et al. Birth weight in relation to leisure time physical activity in adolescence and adulthood: meta-analysis of results from 13 Nordic cohorts. PLoS One. 2009; 4, e8192.CrossRefGoogle ScholarPubMed
9. Hildebrand, M, Kolle, E, Hansen, BH, et al. Association between birth weight and objectively measured sedentary time is mediated by central adiposity: data in 10793 youth from the International Children’s Accelerometry Database. Am J Clin Nutr. 2015; 101, 983990.CrossRefGoogle Scholar
10. Kajantie, E, Strang-Karlsson, S, Hovi, P, et al. Adults born at very low birth weight exercise less than their peers born at term. J Pediatr. 2010; 157, 610616.e611.CrossRefGoogle ScholarPubMed
11. Salonen, MK, Kajantie, E, Osmond, C, et al. Prenatal and childhood growth and leisure time physical activity in adult life. Eur J Public Health. 2011; 21, 719724.CrossRefGoogle ScholarPubMed
12. Ridgway, CL, Brage, S, Sharp, SJ, et al. Does birth weight influence physical activity in youth? A combined analysis of four studies using objectively measured physical activity. PLoS One. 2011; 6, e16125.CrossRefGoogle ScholarPubMed
13. Bassuk, SS, Manson, JE. Epidemiological evidence for the role of physical activity in reducing risk of type 2 diabetes and cardiovascular disease. J Appl Physiol. 2005; 99, 11931204.CrossRefGoogle ScholarPubMed
14. Laine, MK, Eriksson, JG, Kujala, UM, et al. A former career as a male elite athlete – does it protect against type 2 diabetes in later life? Diabetologia. 2014; 57, 270274.CrossRefGoogle ScholarPubMed
15. Colberg, SR, Sigal, RJ, Fernhall, B, et al. Exercise and type 2 diabetes: the American College of Sports Medicine and the American Diabetes Association: joint position statement executive summary. Diabetes Care. 2010; 33, 26922696.CrossRefGoogle ScholarPubMed
16. Fernandes, RA, Zanesco, A. Early physical activity promotes lower prevalence of chronic diseases in adulthood. Hypertens Res. 2010; 33, 926931.CrossRefGoogle ScholarPubMed
17. Whincup, PH, Kaye, SJ, Owen, CG, et al. Birth weight and risk of type 2 diabetes: a systematic review. JAMA. 2008; 300, 28862897.Google ScholarPubMed
18. Newsome, CA, Shiell, AW, Fall, CH, et al. Is birth weight related to later glucose and insulin metabolism? – a systematic review. Diabet Med. 2003; 20, 339348.CrossRefGoogle ScholarPubMed
19. Forsén, T, Eriksson, J, Tuomilehto, J, et al. The fetal and childhood growth of persons who develop type 2 diabetes. Ann Intern Med. 2000; 133, 176182.CrossRefGoogle ScholarPubMed
20. Lussana, F, Painter, RC, Ocke, MC, et al. Prenatal exposure to the Dutch famine is associated with a preference for fatty foods and a more atherogenic lipid profile. Am J Clin Nutr. 2008; 88, 16481652.CrossRefGoogle Scholar
21. Raisanen, S, Gissler, M, Sankilampi, U, et al. Contribution of socioeconomic status to the risk of small for gestational age infants – a population-based study of 1,390,165 singleton live births in Finland. Int J Equity Health. 2013; 12, 28.CrossRefGoogle Scholar
22. Hayward, I, Malcoe, L, Cleathero, L, et al. Investigating maternal risk factors as potential targets of intervention to reduce socioeconomic inequality in small for gestational age: a population-based study. BMC Public Health. 2012; 12, 113.CrossRefGoogle ScholarPubMed
23. Boone-Heinonen, J, Diez Roux, AV, Kiefe, CI, et al. Neighborhood socioeconomic status predictors of physical activity through young to middle adulthood: the CARDIA study. Soc Sci Med. 2011; 72, 641649.CrossRefGoogle Scholar
24. Stalsberg, R, Pedersen, AV. Effects of socioeconomic status on the physical activity in adolescents: a systematic review of the evidence. Scand J Med Sci Sports. 2010; 20, 368383.CrossRefGoogle ScholarPubMed
25. Vickers, MH, Breier, BH, McCarthy, D, Gluckman, PD. Sedentary behavior during postnatal life is determined by the prenatal environment and exacerbated by postnatal hypercaloric nutrition. Am J Physiol Regul Integr Comp Physiol. 2003; 285, R271R273.CrossRefGoogle ScholarPubMed
26. Cunha Fda, S, Dalle Molle, R, Portella, AK, et al. Both food restriction and high-fat diet during gestation induce low birth weight and altered physical activity in adult rat offspring: the ‘Similarities in the Inequalities’ model. PLoS One. 2015; 10, e0118586.CrossRefGoogle ScholarPubMed
27. Bellinger, L, Sculley, DV, Langley-Evans, SC. Exposure to undernutrition in fetal life determines fat distribution, locomotor activity and food intake in ageing rats. Int J Obes. 2006; 30, 729738.CrossRefGoogle ScholarPubMed
28. Donovan, EL, Hernandez, CE, Matthews, LR, et al. Periconceptional undernutrition in sheep leads to decreased locomotor activity in a natural environment. J Dev Orig Health Dis. 2013; 4, 296299.CrossRefGoogle Scholar
29. Williams, PJ, Kurlak, LO, Perkins, AC, et al. Hypertension and impaired renal function accompany juvenile obesity: the effect of prenatal diet. Kidney Int. 2007; 72, 279289.CrossRefGoogle ScholarPubMed
30. Todd, SE, Oliver, MH, Jaquiery, AL, Bloomfield, FH, Harding, JE. Periconceptional undernutrition of ewes impairs glucose tolerance in their adult offspring. Pediatr Res. 2009; 65, 409413.CrossRefGoogle ScholarPubMed
31. Gopalakrishnan, GS, Gardner, DS, Dandrea, J, et al. Influence of maternal pre-pregnancy body composition and diet during early-mid pregnancy on cardiovascular function and nephron number in juvenile sheep. Br J Nutr. 2005; 94, 938947.CrossRefGoogle ScholarPubMed
32. Alexander, G. Studies on the placenta of the sheep (Ovis aries L.) – effect of surgical reduction in the number of caruncles. J Reprod Fertil. 1964; 7, 307322.CrossRefGoogle ScholarPubMed
33. 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 Dev Physiol. 1979; 1, 379398.Google ScholarPubMed
34. Owens, JA, Falconer, J, Robinson, JS. Effect of restriction of placental growth on oxygen delivery to and consumption by the pregnant uterus and fetus. J Dev Physiol. 1987; 9, 137150.Google ScholarPubMed
35. Owens, JA, Falconer, J, Robinson, JS. Effect of restriction of placental growth on umbilical and uterine blood flows. Am J Physiol Regul Integr Comp Physiol. 1986; 250(Pt 2), R427R434.CrossRefGoogle ScholarPubMed
36. Owens, JA, Falconer, J, Robinson, JS. Glucose metabolism in pregnant sheep when placental growth is restricted. Am J Physiol Regul Integr Comp Physiol. 1989; 257(Pt 2), R350R357.CrossRefGoogle ScholarPubMed
37. Owens, JA, Falconer, J, Robinson, JS. Restriction of placental size in sheep enhances efficiency of placental transfer of antipyrine, 3-O-methyl-D-glucose but not of urea. J Dev Physiol. 1987; 9, 457464.Google Scholar
38. Gatford, KL, Clarke, IJ, De Blasio, MJ, et al. Perinatal growth and plasma GH profiles in adolescent and adult sheep. J Endocrinol. 2002; 173, 151159.CrossRefGoogle ScholarPubMed
39. Wooldridge, AL, Bischof, RJ, Meeusen, EN, et al. Placental restriction of fetal growth reduces cutaneous responses to antigen after sensitization in sheep. Am J Physiol Regul Integr Comp Physiol. 2014; 306, R441R446.CrossRefGoogle ScholarPubMed
40. De Blasio, MJ, Gatford, KL, Harland, ML, Robinson, JS, Owens, JA. Placental restriction reduces insulin sensitivity and expression of insulin signaling and glucose transporter genes in skeletal muscle, but not liver, in young sheep. Endocrinology. 2012; 153, 21422151.CrossRefGoogle Scholar
41. 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, R875R886.CrossRefGoogle ScholarPubMed
42. 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. 2007; 148, 13501358.CrossRefGoogle ScholarPubMed
43. Gatford, KL, Mohammad, SN, Harland, ML, et al. Impaired beta-cell function and inadequate compensatory increases in beta-cell mass after intrauterine growth restriction in sheep. Endocrinology. 2008; 149, 51185127.CrossRefGoogle ScholarPubMed
44. National Health and Medical Research Council of Australia. Australian Code of Practice for the Care and Use of Animals for Scientific Purposes, 8th edn, 2013. Australian Government Publishing Service: Canberra.Google Scholar
45. Morton, AJ, Rudiger, SR, Wood, NI, et al. Early and progressive circadian abnormalities in Huntington’s disease sheep are unmasked by social environment. Hum Mol Genet. 2014; 23, 33753383.CrossRefGoogle ScholarPubMed
46. Verbyla, AP, Cullis, BR, Kenward, MG, Welham, SJ. The analysis of designed experiments and longitudinal data by using smoothing splines. J R Stat Soc Ser C Appl Stat. 1999; 48, 269311.CrossRefGoogle Scholar
47. Tobler, I, Jaggi, K, Arendt, J, Ravault, JP. Long-term 24-hour rest-activity pattern of sheep in stalls and in the field. Experientia. 1991; 47, 744749.CrossRefGoogle ScholarPubMed
48. Zumwalt, A. The effect of endurance exercise on the morphology of muscle attachment sites. J Exp Biol. 2006; 209(Pt 3), 444454.CrossRefGoogle ScholarPubMed
49. Clifton, VL. Review: sex and the human placenta: mediating differential strategies of fetal growth and survival. Placenta. 2010; 31(Suppl.), S33S39.CrossRefGoogle ScholarPubMed
50. Hsu, Y-WA, Wang, SD, Wang, S, et al. Role of the dorsal medial habenula in the regulation of voluntary activity, motor function, hedonic state, and primary reinforcement. J Neurosci. 2014; 34, 1136611384.CrossRefGoogle ScholarPubMed
51. Rowland, TW. The biological basis of physical activity. Med Sci Sports Exerc. 1998; 30, 392399.CrossRefGoogle ScholarPubMed
52. Thorburn, AW, Proietto, J. Biological determinants of spontaneous physical activity. Obes Rev. 2000; 1, 8794.CrossRefGoogle ScholarPubMed
53. DiPietro, L. Physical activity, body weight, and adiposity: an epidemiologic perspective. Exerc Sport Sci Rev. 1995; 23, 275303.CrossRefGoogle ScholarPubMed
54. Stults-Kolehmainen, MA, Sinha, R. The effects of stress on physical activity and exercise. Sports Med. 2014; 44, 81121.CrossRefGoogle ScholarPubMed
55. Allden, W, McDWhittaker, I. The determinants of herbage intake by grazing sheep: the interrelationship of factors influencing herbage intake and availability. Aust J Agric Res. 1970; 21, 755766.CrossRefGoogle Scholar
56. 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 Endocrinol Metab. 2000; 279, E83E87.CrossRefGoogle ScholarPubMed
57. Ainslie, DA, Morris, MJ, Wittert, G, et al. Estrogen deficiency causes central leptin insensitivity and increased hypothalamic neuropeptide Y. Int J Obes Relat Metab Disord. 2001; 25, 16801688.CrossRefGoogle ScholarPubMed
58. Poehlman, ET, Tchernof, A. Traversing the menopause: changes in energy expenditure and body composition. Coron Artery Dis. 1998; 9, 799803.CrossRefGoogle ScholarPubMed
59. Nieto, CAR, Ferguson, MB, Macleay, CA, et al. Selection for superior growth advances the onset of puberty and increases reproductive performance in ewe lambs. Animal. 2013; 7, 990997.CrossRefGoogle Scholar
60. Dahan-Oliel, N, Mazer, B, Majnemer, A. Preterm birth and leisure participation: a synthesis of the literature. Res Dev Disabil. 2012; 33, 12111220.CrossRefGoogle ScholarPubMed
61. Winfield, CG, Syme, GJ, Pearson, AJ. Effect of familiarity with each other and breed on the spatial behaviour of sheep in an open field. Appl Anim Ethol. 1981; 7, 6775.CrossRefGoogle Scholar
62. 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, 644653.CrossRefGoogle ScholarPubMed
63. Rattray, PV, Garrett, WN, East, NE, Hinman, N. Growth, development and composition of the ovine conceptus and mammary gland during pregnancy. J Anim Sci. 1974; 38, 613626.CrossRefGoogle ScholarPubMed
64. 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, 12731285.CrossRefGoogle ScholarPubMed
65. Spencer, TE, Hansen, TR. Implantation and establishment of pregnancy in ruminants. Adv Anat Embryol Cell Biol. 2015; 216, 105135.CrossRefGoogle ScholarPubMed
66. Vonnahme, KA, Evoniuk, J, Johnson, ML, et al. Placental vascularity and growth factor expression in singleton, twin, and triplet pregnancies in the sheep. Endocrine. 2008; 33, 5361.CrossRefGoogle ScholarPubMed
67. Roseboom, TJ, Painter, RC, van Abeelen, AF, Veenendaal, MV, de Rooij, SR. Hungry in the womb: what are the consequences? Lessons from the Dutch famine. Maturitas. 2011; 70, 141145.CrossRefGoogle ScholarPubMed
Supplementary material: File

Kaur supplementary material

Supplementary Table

Download Kaur supplementary material(File)
File 17.5 KB