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Bone growth and sexual dimorphism at birth in intrauterine-growth-retarded rats

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Abstract

This paper addresses the effect of a reduction of uterine blood flow (RUB) on postcranial bone growth in rats. The objectives were: (1) to discover and characterize the changes evoked by growth retardation through a reduction in placental blood flow, (2) to see if the resulting growth retardation is different in each bone, and (3) to analyze any sex-specific features. RUB was induced by the partial bending of uterine vessels at day 1 of pregnancy. Control and sham-operated animals were also included. The animals were X-rayed at birth. The lengths and widths of the humerus, radius, and femur and pelvic length, interischial, interpubic, and pubic widths were measured. Data were analyzed by ANOVA and LSD post hoc tests. The intersubject analysis showed significant differences between groups and non-significant differences between sexes. In males, sham-operated and RUB showed significant differences in pelvic lengths and widths, and humeral, radial, femoral, and tibial widths. In females, there were significant differences only for humeral widths, radial lengths and widths, and femoral and tibial widths. We conclude that reduced blood flow delays appendicular bone growth as observed at birth. Pelvic length was more affected than that of the limbs. The widths of the pelvic and limbs bones, in turn, were more altered than the lengths, and the growth of the males more than that of the females. Partial bending of uterine vessels compromised postcranial growth, though under such disadvantageous circumstances the females proved to be more capable of growing and thus more resilient than the males.

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References

  • Adams P (1969) The effects of experimental protein deficiency on the growth and development of long bones. In: Jelliffe AM (ed) Symposium Ossium. Livingstone, Edinburgh

  • Adams P, Berridge FR (1969) Effects of kwashiorkor on cortical and trabecular bone. Arch Dis Child 44:705

    Article  PubMed  CAS  Google Scholar 

  • Barker DJP (1998) In utero programming of chronic disease. Clin Sci 95:115–128

    Article  PubMed  CAS  Google Scholar 

  • Beltrand J, Alison M, Nicolescu R, Verkauskiene R, Deghmoun S, Sibony O, Sebag G, Le’Vy Marchal C (2008) Bone mineral content at birth is determined both by birth weight and fetal growth pattern. Pediatr Res 64:1–8

    Article  Google Scholar 

  • Berdnikovs S, Bernstein M, Metzler A, German RZ (2007) Pelvic growth: ontogeny of size and shape sexual dimorphism in rat pelves. J Morphol 268:12–22

    Article  PubMed  CAS  Google Scholar 

  • Bernstein P, Crelin ES (2005) Bony pelvic sexual dimorphism in the rat. Anat Rec 157:517–525

    Article  Google Scholar 

  • Cameron GN, Eshelman BD (1996) Growth and reproduction of hispid cotton rats (Sigmodon hispidus) in response to naturally occurring levels of dietary protein. J Mammal 77:220–231

    Article  Google Scholar 

  • Cesani MF, Orden AB, Zucchi M, Muñe MC, Oyhenart EE, Pucciarelli HM (2006) Effect of undernutrition on the cranial growth of the rat. An intergenerational study. J Anat 209:137–147

    Article  PubMed  Google Scholar 

  • Chaddha V, Viero S, Huppertz B, Kingdom J (2004) Developmental biology of the placenta and the origins of placental insufficiency. Semin Fetal Neonatal Med 9:357–369

    Article  PubMed  Google Scholar 

  • Dammrich K (1991) Relationship between nutrition and bone growth in large and giant dogs. J Nutr 121:114–121

    Google Scholar 

  • Desai M, Crowther NJ, Lucas A, Hales CN (1996) Organ-selective growth in the offspring of protein-restricted mothers. Br J Nutr 76:591–603

    Article  PubMed  CAS  Google Scholar 

  • Dressino V, Orden B, Oyhenart EE (2002) Sexual responses to intrauterine stress: body and brain growth. Clin Exp Obstet Gynecol 29:100–102

    PubMed  CAS  Google Scholar 

  • Gicquel C, Le Bouc Y (2006) Hormonal regulation of fetal growth. Horm Res 65:28–33

    Article  PubMed  CAS  Google Scholar 

  • Guimarey LM, Oyhenart EE, Quintero FA, Fucini MC (2003) Body weight recovery in intrauterine growth-retarded rats treated with growth hormone. Clin Exp Obstet Gynecol 30:51–56

    PubMed  CAS  Google Scholar 

  • Huizinga CT, Engelbregt MJT, Rekers-Mombarg LTM, Vaessen SFC, Delemarre-van de Waal HA, Fodor M (2004) Ligation of the uterine artery and early postnatal food restriction—animal models for growth retardation. Horm Res 62:233–240

    Article  PubMed  CAS  Google Scholar 

  • Loveridge N, Noble BS (1994) Control of longitudinal growth: the role of nutrition. Eur J Clin Nutr 48:75–84

    PubMed  CAS  Google Scholar 

  • McCance RA (1960) Severe undernutrition in growing and adult animals. 1. Production and general effects. Br J Nutr 14:59–68

    Article  CAS  Google Scholar 

  • McMillen C, Adams MB, Ross JT, Coulter CL, Simonetta G, Owens JA, Robinson JS, Edwards LJ (2001) Fetal growth restriction: adaptations and consequences. Reproduction 122:195–204

    Article  PubMed  CAS  Google Scholar 

  • Miller JP, German RZ (1999) Protein malnutrition affects the growth trajectories of the craniofacial skeleton in rats. J Nutr 129:2061–2069

    PubMed  CAS  Google Scholar 

  • Morrison JL (2008) Sheep model of intrauterine growth restriction: fetal adaptations and consequences. Clin Experim Pharmacol Physiol 35:730–743

    Article  CAS  Google Scholar 

  • Mughal MZ, Ross R, Tsang RC (1989) Clearance of calcium across in situ perfused placentas in intrauterine growth-retarded rat fetuses. Pediatr Res 24:420–422

    Article  Google Scholar 

  • Myatt L (2006) Placental adaptive responses and fetal programming. J Physiol 572:25–30

    PubMed  CAS  Google Scholar 

  • Nafee TM, Farrell WE, Carroll WD, Fryer AA, Ismail KM (2008) Epigenetic control of fetal gene expression. BJOG 115:158–168

    PubMed  CAS  Google Scholar 

  • Namgung R, Tsang RC (2000) Factors affecting newborn bone mineral content: in utero effects on newborn bone mineralization. Proc Nutr Soc 59:55–63

    Article  PubMed  CAS  Google Scholar 

  • Oyhenart EE, Muñe MC, Pucciarelli HM (1998) Influence of intrauterine blood supply on cranial growth and sexual dimorphism at birth. Growth Dev Aging 62:187–198

    PubMed  CAS  Google Scholar 

  • Oyhenart EE, Guimarey LM, Fucini MC, Quintero FA, Orden B (2002) Effects of bilateral uterine vessel ligation on skeletal growth in rats. Clin Exp Obstet Gynecol 29:121–125

    PubMed  CAS  Google Scholar 

  • Prader A, Tanner JM, Harnack GAV (1963) Catch-up growth following illness or starvation. An example of developmental canalization in man. J Pediatr 62:646–659

    Article  PubMed  CAS  Google Scholar 

  • Schreuder MF, Fodor M, van Wijk JA, Delemarre-van de Waal HA (2006) Association of birth weight with cardiovascular parameters in adult rats during baseline and stressed conditions. Pediatr Res 59:126–130

    Article  PubMed  Google Scholar 

  • Stewart RJ, Preece RF, Sheppard HG (1975) Twelve generations of marginal protein deficiency. Br J Nutr 33:233–253

    Article  PubMed  CAS  Google Scholar 

  • Tanner JM (1962) Growth at adolescense. Blackwell, Oxford

    Google Scholar 

  • Widdowson EM, McCance RA (1963) The effect of finite periods of undernutrition at different ages on the composition and subsequent development of the rat. Proc R Soc Lond B Biol Sci 185:329–342

    Article  Google Scholar 

  • Wigglesworth JS (1964) Experimental growth retardation of foetal rat. J Pathol Bacteriol 88:1–13

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This research was supported by grants from the Universidad Nacional de La Plata (UNLP) and the Consejo Nacional de Investigaciones Científicas y Técnicas (CONICET). The authors are grateful to Dr. Donald F. Haggerty, a native English speaker, for editing the manuscript.

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Correspondence to Evelia Edith Oyhenart.

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Oyhenart, E.E., Cesani, M.F., Castro, L.E. et al. Bone growth and sexual dimorphism at birth in intrauterine-growth-retarded rats. Anat Sci Int 86, 119–127 (2011). https://doi.org/10.1007/s12565-010-0098-y

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  • DOI: https://doi.org/10.1007/s12565-010-0098-y

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