Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-19T10:29:40.565Z Has data issue: false hasContentIssue false
  • English
  • Français

Spontaneous intrauterine growth restriction due to increased litter size in the guinea pig programmes postnatal growth, appetite and adult body composition

Published online by Cambridge University Press:  23 June 2016

D. M. Horton ,
D. A. Saint ,
J. A. Owens ,
K. L. Kind  and
K. L. Gatford Open the ORCID record for K. L. Gatford [Opens in a new window]
D. M. Horton
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia School of Medicine, The University of Adelaide, SA, Australia
D. A. Saint
Affiliation:
School of Medicine, The University of Adelaide, SA, Australia
J. A. Owens
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia School of Medicine, The University of Adelaide, SA, Australia
K. L. Kind
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia School of Animal and Veterinary Sciences, The University of Adelaide, SA, Australia
K. L. Gatford*
Affiliation:
Robinson Research Institute, The University of Adelaide, SA, Australia School of Medicine, The University of Adelaide, SA, Australia
*
*Address for correspondence: Dr K. L. Gatford, Discipline of Obstetrics and Gynaecology, School of Medicine, University of Adelaide, SA 5005, Australia. (Email Kathy.gatford@adelaide.edu.au)
Get access Rights & Permissions [Opens in a new window]

Abstract

Intrauterine growth restriction (IUGR) and subsequent neonatal catch-up growth are implicated in the programming of increased appetite, adiposity and cardiometabolic diseases. Guinea pigs provide an alternate small animal model to rodents to investigate mechanisms underlying prenatal programming, being relatively precocial at birth, with smaller litter sizes and undergoing neonatal catch-up growth after IUGR. The current study, therefore, investigated postnatal consequences of spontaneous IUGR due to varying litter size in this species. Size at birth, neonatal, juvenile (post-weaning, 30–60 days) and adolescent (60–90 days) growth, juvenile and adolescent food intake, and body composition of young adults (120 days) were measured in 158 male and female guinea pigs from litter sizes of one to five pups. Compared with singleton pups, birth weight of pups from litters of five was reduced by 38%. Other birth size measures were reduced to lesser degrees with head dimensions being relatively conserved. Pups from larger litters had faster fractional neonatal growth and faster absolute and fractional juvenile growth rates (P<0.005 for all). Relationships of post-weaning growth, feed intakes and adult body composition with size at birth and neonatal growth rate were sex specific, with neonatal growth rates strongly and positively correlated with adiposity in males only. In conclusion, spontaneous IUGR due to large litter sizes in the guinea pig causes many of the programmed sequelae of IUGR reported in other species, including human. This may therefore be a useful model to investigate the mechanisms underpinning perinatal programming of hyperphagia, obesity and longer-term metabolic consequences.

Keywords

adiposityappetiteguinea piglitter sizesex differences
Type
Original Article
Information
Journal of Developmental Origins of Health and Disease , Volume 7 , Issue 5: Themed Issue: Australia/New Zealand 2015 DOHaD Scientific Meeting: Advances and Updates , October 2016 , pp. 548 - 562
Check for updates
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. Barker, DJ, Hales, CN, Fall, CH, et al. Type 2 (non-insulin-dependent) diabetes mellitus, hypertension and hyperlipidaemia (syndrome X): relation to reduced fetal growth. Diabetologia. 1993; 36, 62–67.Google Scholar
2. Gluckman, PD, Hanson, MA. Living with the past: evolution, development, and patterns of disease. Science. 2004; 305, 1733–1736.Google Scholar
3. Kind, KL, Simonetta, G, Clifton, PM, Robinson, JS, Owens, JA. Effect of maternal feed restriction on blood pressure in the adult guinea pig. Exp Physiol. 2002; 87, 469–477.CrossRefGoogle ScholarPubMed
4. Kind, KL, Simonetta, G, Clifton, PM, et al. Effect of maternal feed restriction on glucose tolerance in the adult guinea pig. Am J Physiol. 2003; 284, R140–R152.Google Scholar
5. Kind, KL, Clifton, PM, Katsman, AI, et al. Restricted fetal growth and the response to dietary cholesterol in the guinea pig. Am J Physiol. 1999; 277, R1675–R1682.Google Scholar
6. Bertin, E, Gangnerau, M, Bailbe, D, Portha, B. Glucose metabolism and beta-cell mass in adult offspring of rats protein and/or energy restricted during the last week of pregnancy. Am J Physiol. 1999; 277, E11–E17.Google Scholar
7. 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
8. Fernandez-Twinn, DS, Wayman, A, Ekizoglou, S, et al. Maternal protein restriction leads to hyperinsulinemia and reduced insulin-signaling protein expression in 21-mo-old female rat offspring. Am J Physiol. 2005; 288, 368–373.Google Scholar
9. Ozanne, SE, Hales, CN. Poor fetal growth followed by rapid postnatal catch-up growth leads to premature death. Mech Ageing Dev. 2005; 126, 852–854.Google Scholar
10. Woods, LL, Weeks, DA, Rasch, R. Programming of adult blood pressure by maternal protein restriction: role of nephrogenesis. Kidney Int. 2004; 65, 1339–1348.Google Scholar
11. Desai, M, Crowther, NJ, Lucas, A, Hales, CN. Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr. 1996; 76, 591–603.Google Scholar
12. Bleker, OP, Buimer, M, van der Post, JAM, van der Veen, F. Ted (G.J.) Kloosterman: on intrauterine growth. The significance of prenatal care. Studies on birth weight, placental weight and placental index. Placenta. 2006; 27, 1052–1054.Google Scholar
13. Pardi, G, Marconi, AM, Cetin, I. Pathophysiology of intrauterine growth retardation: role of the placenta. Acta Paediatr Suppl. 1997; 423, 170–172.Google Scholar
14. Simmons, R, Templeton, L, Gertz, S. Intrauterine growth retardation leads to the development of type 2 diabetes in the rat. Diabetes. 2001; 50, 2279–2286.Google Scholar
15. Engelbregt, MJT, van Weissenbruch, MM, Lips, P, et al. Body composition and bone measurements in intra-uterine growth retarded and early postnatally undernourished male and female rats at the age of 6 months: comparison with puberty. Bone. 2004; 34, 180–186.Google Scholar
16. Jansson, T, Lambert, GW. Effect of intrauterine growth restriction on blood pressure, glucose tolerance and sympathetic nervous activity in the rat at 3-4 months of age. J Hypertens. 1999; 17, 1239–1248.Google Scholar
17. Houdijk, E, Engelbregt, M, Popp-Snijders, C, Delemarre-Van der Waal, H. Endocrine regulation and extended follow up of longitudinal growth in intrauterine growth-retarded rats. J Endocrinol. 2000; 166, 599–608.Google Scholar
18. Eriksson, JG, Forsen, T, Tuomilehto, J, Osmond, C, Barker, DJ. Size at birth, childhood growth and obesity in adult life. Int J Obes Relat Metab Disord. 2001; 25, 735–740.Google Scholar
19. Eriksson, JG, Forsen, T, Tuomilehto, J, et al. Catch-up growth in childhood and death from coronary heart disease: longitudinal study. Br Med J. 1999; 318, 427–431.Google Scholar
20. Law, CM, Shiell, AW, Newsome, CA, et al. Fetal, infant and childhood growth and adult blood pressure: a longitudinal study from birth to 22 years of age. Circulation. 2002; 105, 1088–1092.Google Scholar
21. Fagerberg, B, Bondjers, L, Nilsson, P. Low birth weight in combination with catch-up growth predicts the occurrence of the metabolic syndrome in men at middle age: the Atherosclerosis and Insulin Resistance study. J Intern Med. 2004; 256, 254–259.Google Scholar
22. Eckstein, P, McKeown, T. The influence of maternal age, parity and weight on litter size in the guinea-pig. J Endocrinol. 1955; 12, 115–119.Google Scholar
23. Eckstein, P, McKeown, T, Record, RG. Variation in placental weight according to litter size in the guinea-pig. J Endocrinol. 1955; 12, 108–114.Google Scholar
24. Engle, WA, Lemons, JA. Composition of the fetal and maternal guinea pig throughout gestation. Pediatr Res. 1986; 20, 1156–1160.Google Scholar
25. Arbeeny, CM, Nordin, C, Edelstein, D, et al. Hyperlipoproteinemia in spontaneous diabetic guinea pigs. Metabolism. 1989; 38, 895–900.Google Scholar
26. Vannevel, J. Diabetes mellitus in a 3-year-old, intact, female guinea pig. Can Vet J. 1998; 39, 503.Google Scholar
27. Kind, KL, Roberts, CT, Sohlstrom, A, et al. Chronic maternal feed restriction impairs growth but increases adiposity of the fetal guinea pig. Am J Physiol. 2005; 288, R119–R126.Google Scholar
28. Roberts, CT, Sohlstrom, A, Kind, KL, et al. Maternal food restriction reduces the exchange surface area and increases the barrier thickness of the placenta in the guinea-pig. Placenta. 2001; 22, 177–186.Google Scholar
29. Roberts, CT, Sohlstrom, A, Kind, KL, et al. Altered placental structure induced by maternal food restriction in guinea pigs: a role for circulating IGF-II and IGFBP-2 in the mother? Placenta . 2001; 22(Suppl. A), S77–S82.CrossRefGoogle ScholarPubMed
30. Gilbert, JS, Nijland, MJ. Sex differences in the developmental origins of hypertension and cardiorenal disease. Am J Physiol. 2008; 295, R1941–R1952.Google Scholar
31. Sarr, O, Thompson, JA, Zhao, L, Lee, TY, Regnault, TRH. Low birth weight male guinea pig offspring display increased visceral adiposity in early adulthood. PLoS One. 2014; 9, e98433.Google Scholar
32. Palliser, HK, Kelleher, MA, Welsh, TN, Zakar, T, Hirst, JJ. Mechanisms leading to increased risk of preterm birth in growth-restricted guinea pig pregnancies. Reprod Sci. 2014; 21, 269–276.Google Scholar
33. Turner, AJ, Trudinger, BJ. A modification of the uterine artery restriction technique in the guinea pig fetus produces asymmetrical ultrasound growth. Placenta. 2009; 30, 236–240.CrossRefGoogle ScholarPubMed
34. Ibsen, HL. Prenatal growth in guinea-pigs with special reference to environmental factors affecting weight at birth. J Exp Zool. 1928; 51, 51–94.Google Scholar
35. McKeown, T, MacMahon, B. The influence of litter size and litter order on length of gestation and early postnatal growth in the guinea-pig. J Endocrinol. 1956; 13, 195–200.Google Scholar
36. Sisk, DB. Physiology. In The Biology of the Guinea Pig (eds. Wagner J, Manning P), 1976; pp. 63–98. Acedemic Press: New York.Google Scholar
37. Mittelman, SD, Van Citters, GW, Kirkman, EL, Bergman, RN. Extreme insulin resistance of the central adipose depot in vivo. Diabetes. 2002; 51, 755–761.Google Scholar
38. Lim, KI, Yang, SJ, Kim, TN, et al. The association between the ratio of visceral fat to thigh muscle area and metabolic syndrome: the Korean Sarcopenic Obesity Study (KSOS). Clin Endocrinol. 2010; 73, 588–594.Google Scholar
39. Ong, KK, Ahmed, ML, Emmett, PM, Preece, MA, Dunger, DB. Association between postnatal catch-up growth and obesity in childhood: prospective cohort study. Br Med J. 2000; 320, 967–971.Google Scholar
40. Goy, RW, Hoar, RM, Young, WC. Length of gestation in the guinea pig with data on the frequency and time of abortion and stillbirth. Anat Rec. 1957; 128, 747–757.Google Scholar
41. Sohlstrom, A, Katsman, A, Kind, KL, et al. Food restriction alters pregnancy-associated changes in IGF and IGFBP in the guinea pig. Am J Physiol. 1998; 274(Pt 1), E410–E416.Google Scholar
42. Davis, SR, Mepham, TB, Lock, KL. Relative importance of pre-partum and post-partum factors in the control of milk yield in the guinea-pig. J Dairy Res. 1979; 46, 613–621.Google Scholar
43. Mepham, TB, Beck, NFG. Variation in the yield and composition of milk throughout lactation in the guinea pig (Cavia porcellus). Comp Biochem Physiol A Physiol. 1973; 45, 273–281.Google Scholar
44. Phillips, DI, Barker, DJP, Hales, CN, Hirst, S, Osmond, C. Thinness at birth and insulin resistance in adult life. Diabetologia. 1994; 37, 150–154.Google Scholar
45. Law, CM, Gordon, GS, Shiell, AW, Barker, DJ, Hales, CN. Thinness at birth and glucose tolerance in seven-year-old children. Diabetic Med. 1995; 12, 24–29.Google Scholar
46. Rosenberg, A. The IUGR newborn. Semin Perinatol. 2008; 32, 219–224.Google Scholar
47. Ravelli, ACJ, Vandermeulen, JHP, Michels, RPJ, et al. Glucose tolerance in adults after prenatal exposure to famine. Lancet. 1998; 351, 173–177.Google Scholar
48. 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. 2007; 292, 875–886.Google Scholar
49. Kelleher, MA, Hirst, JJ, Palliser, HK. Changes in neuroactive steroid concentrations after preterm delivery in the guinea pig. Reprod Sci. 2013; 20, 1365–1375.Google Scholar
50. 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.Google Scholar
51. Shin, BC, Dai, Y, Thamotharan, M, Gibson, LC, Devaskar, SU. Pre- and postnatal calorie restriction perturbs early hypothalamic neuropeptide and energy balance. J Neurosci Res. 2012; 90, 1169–1182.Google Scholar
52. Tenovuo, A, Kero, P, Piekkala, P, et al. Growth of 519 small for gestational age infants during the first two years of life. Acta Paediatr Scand. 1987; 76, 636–646.Google Scholar
53. Albertsson Wikland, K, Boguszewski, M, Karlberg, J. Children born small-for-gestational age: postnatal growth and hormonal status. Horm Res. 1998; 49(Suppl. 2), 7–13.Google Scholar
54. Karlberg, J, Albertsson Wikland, K. Growth in full-term small-for-gestational-age infants: from birth to final height. Pediatr Res. 1995; 38, 733–739.Google Scholar
55. Hokken-Koelega, AC, De Ridder, MA, Lemmen, RJ, et al. Children born small for gestational age: do they catch up? Pediatr Res. 1995; 38, 267–271.Google Scholar
56. Holness, MJ, Sugden, MC. Antecedent protein restriction exacerbates development of impaired insulin action after high-fat feeding. Am J Physiol. 1999; 39, E85–E93.Google Scholar
57. Benyshek, DC, Johnston, CS, Martin, JF. Post-natal diet determines insulin resistance in fetally malnourished, low birthweight rats (F1) but diet does not modify the insulin resistance of their offspring (F2). Life Sci. 2004; 74, 3033–3041.Google Scholar
58. Dobson, CC, Mongillo, DL, Brien, DC, et al. Chronic prenatal ethanol exposure increases adiposity and disrupts pancreatic morphology in adult guinea pig offspring. Nutr Diabetes. 2012; 2, e57.Google Scholar
59. Law, CM, Barker, DJ, Osmond, C, Fall, CH, Simmonds, SJ. Early growth and abdominal fatness in adult life. J Epidemiol Commun Health. 1992; 46, 184–186.CrossRefGoogle ScholarPubMed
60. Rogers, I, the EURO-BLCS Study Group. The influence of birthweight and intrauterine environment on adiposity and fat distribution in later life. Int J Obes Relat Metab Disord. 2003; 27, 755–777.Google Scholar
61. Kensara, OA, Wootton, SA, Phillips, DI, et al. Fetal programming of body composition: relation between birth weight and body composition measured with dual-energy X-ray absorptiometry and anthropometric methods in older Englishmen. Am J Clin Nutr. 2005; 82, 980–987.Google Scholar
62. Ravelli, ACJ, van der Meulen, JHP, Osmond, C, Barker, DJP, Bleker, OP. Obesity at the age of 50 y in men and women exposed to famine prenatally. Am J Clin Nutr. 1999; 70, 811–816.Google Scholar