Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter April 7, 2006

Intrauterine growth restriction induces increased capillary density and accelerated type I fiber maturation in newborn pig skeletal muscles

  • Reinhard Bauer , Tomasz Gedrange , Kathrin Bauer and Bernd Walter

Abstract

Aims: Humans with low birth weight exhibit evidences of vascular dysfunction. Recent findings indicate a microvascular rarefaction in skeletal muscles soon after postnatal development in rats suffered by intrauterine protein restriction.

Methods: To examine the effects of intrauterine growth restriction on capillary density, muscle fiber distribution and accompanying muscular and systemic circulation immediately after birth, studies were conducted on 1-day-old anesthetized normal weight (n=7) and intrauterine growth restricted (n=6) piglets. Cardiac output and hind limb muscle blood flow were measured by colored microspheres. Counting of type I fibers and skeletal capillary numbers was done by immunohistochemical staining.

Results: Increased proportion of type I fibers and capillary density was found in the flexor digitalis superficialis and gastrocnemius medialis (P<0.05) in newborn IUGR piglets. Furthermore, a marked correlation was shown between capillary density and type I fiber fraction for all flexor muscles studied (P<0.05). Moreover, cardiac output and muscular blood flow were markedly increased in IUGR piglets (P<0.05). Correspondingly, total peripheral resistance, as well as vascular resistance, of hind limb flexors appeared significantly decreased (P<0.05).

Conclusions: Compromised intrauterine environmental conditions leading to fetal growth restriction provokes coordinated structural and functional adaptation of skeletal muscles.

:

Corresponding author: Dr Reinhard Bauer Institute for Molecular Cell Biology, Pathophysiology Lab Universitätsklinikum Jena Friedrich Schiller University D-07740 Jena[ep Germany Tel.: +49 (3641) 938956 Fax: +49 (3641) 938954

References

1 Aberle ED: Myofiber differentiation in skeletal muscles of newborn runt and normal weight pigs. J Anim Sci59 (1984) 165110.2527/jas1984.5961651xSearch in Google Scholar

2 Aplin J: Maternal influences on placental development. Semin Cell Dev Biol11 (2000) 11510.1006/scdb.2000.0157Search in Google Scholar

3 Barker DJP: Mother, babies, and health in later life. Churchill Livingstone, Edinburgh 199810.1016/S0033-3506(99)00170-5Search in Google Scholar

4 Bauer R, B Walter, E Gaser, T Rosel, H Kluge, U Zwiener: Cardiovascular function and brain metabolites in normal weight and intrauterine growth restricted newborn piglets – effect of mild hypoxia. Exp Toxicol Pathol50 (1998) 294Search in Google Scholar

5 Bauer R, B Walter, A Hoppe, E Gaser, V Lampe, E Kauf, U Zwiener: Body weight distribution and organ size in newborn swine (sus scrofa domestica) – a study describing an animal model for asymmetrical intrauterine growth retardation. Exp Toxicol Pathol50 (1998) 59Search in Google Scholar

6 Bauer R, B Walter, R Vollandt, U Zwiener: Intrauterine growth restriction ameliorates the effects of gradual hemorrhagic hypotension on regional cerebral blood flow and brain oxygen uptake in newborn piglets. Pediatr Res56 (2004) 639Search in Google Scholar

7 Bauer R, B Walter, E Wurker, H Kluge, U Zwiener: Colored microsphere technique as a new method for quantitative-multiple estimation of regional hepatic and portal blood flow. Exp Toxicol Pathol48 (1996) 415Search in Google Scholar

8 Bauer R, B Walter, U Zwiener: Effect of severe normocapnic hypoxia on renal function in growth-restricted newborn piglets. Am J Physiol Regul Integr Comp Physiol279 (2000) R101010.1152/ajpregu.2000.279.3.R1010Search in Google Scholar PubMed

9 Bauer R, V Wank, B Walter, R Blickhan, U Zwiener: Reduced muscle vascular resistance in intrauterine growth restricted newborn piglets. Exp Toxicol Pathol52 (2000) 271Search in Google Scholar

10 Creasy RK, R Resnik: Intrauterine growth restriction. In: Creasy RK, R Resnik: Maternal-Fetal Medicine. Saunders, Philadelphia 1999Search in Google Scholar

11 De Roth L, HG Downie: Evaluation of viability of neonatal swine. Can Vet J17 (1976) 275Search in Google Scholar

12 Dwyer CM, NC Stickland: Does the anatomical location of a muscle affect the influence of undernutrition on muscle fibre number? J Anat181 (Pt 2) (1992) 373Search in Google Scholar

13 Eisenhauer CL, LS Matsuda, CF Uyehara: Normal physiologic values of neonatal pigs and the effects of isoflurane and pentobarbital anesthesia. Lab Anim Sci44 (1994) 245Search in Google Scholar

14 Gluckman PD, MA Hanson: Living with the past: evolution, development, and patterns of disease. Science305 (2004) 1733Search in Google Scholar

15 Hales CN, DJ Barker, PM Clark, LJ Cox, C Fall, C Osmond, PD Winter: Fetal and infant growth and impaired glucose tolerance at age 64. Br Med J303 (1991) 1019Search in Google Scholar

16 Klockgether-Radke AP, A Frerichs, D Kettler, G Hellige: Propofol and thiopental attenuate the contractile response to vasoconstrictors in human and porcine coronary artery segments. Eur J Anaesthesiol17 (2000) 485Search in Google Scholar

17 Langley-Evans SC, AA Jackson: Captopril normalises systolic blood pressure in rats with hypertension induced by fetal exposure to maternal low protein diets. Comp Biochem Physiol A Physiol110 (1995) 223Search in Google Scholar

18 Lee JC, JC Werner, SE Downing: Adrenal contribution to cardiac responses elicited by acute hypoxia in piglets. Am J Physiol239 (1980) H75110.1152/ajpheart.1980.239.6.H751Search in Google Scholar PubMed

19 Lefaucheur L, P Ecolan, YM Barzic, J Marion, J Le Dividich: Early postnatal food intake alters myofiber maturation in pig skeletal muscle. J Nutr133 (2003) 140Search in Google Scholar

20 Lefaucheur L, P Ecolan, L Plantard, N Gueguen: New insights into muscle fiber types in the pig. J Histochem Cytochem50 (2002) 719Search in Google Scholar

21 Lefaucheur L, F Edom, P Ecolan, GS Butler-Browne: Pattern of muscle fiber type formation in the pig. Dev Dyn203 (1995) 27Search in Google Scholar

22 Leon DA, HO Lithell, D Vagero, I Koupilova, R Mohsen, L Berglund, UB Lithell, PM McKeigue: Reduced fetal growth rate and increased risk of death from ischaemic heart disease: cohort study of 15 000 Swedish men and women born 1915–29. Br Med J317 (1998) 241Search in Google Scholar

23 Lerman J, JP Oyston, TM Gallagher, K Miyasaka, GA Volgyesi, FA Burrows: The minimum alveolar concentration (MAC) and hemodynamic effects of halothane, isoflurane, and sevoflurane in newborn swine. Anesthesiology73 (1990) 717Search in Google Scholar

24 Lin CC, MI Evans: Part 1: Basic considerations. Introduction. In: Lin CC, MI Evans: Intrauterine growth retardation: pathophysiology and clinical management. McGraw-Hill Book Company, New York 1984Search in Google Scholar

25 Makowski EL, G Meschia, W Droegemueller, FC Battaglia: Measurement of umbilical arterial blood flow to the sheep placenta and fetus in utero. Distribution to cotyledons and the intercotyledonary chorion. Circ Res23 (1968) 623Search in Google Scholar

26 Naeye RL, JA Kelly: Judgment of fetal age. 3. The pathologist's evaluation. Pediatr Clin North Am13 (1966) 849Search in Google Scholar

27 Narusawa M, RB Fitzsimons, S Izumo, B Nadal-Ginard, NA Rubinstein, AM Kelly: Slow myosin in developing rat skeletal muscle. J Cell Biol104 (1987) 447Search in Google Scholar

28 Newsome CA, AW Shiell, CH Fall, DI Phillips, R Shier, CM Law: Is birth weight related to later glucose and insulin metabolism?– a systematic review. Diabet Med20 (2003) 339Search in Google Scholar

29 Ozanne SE, GS Olsen, LL Hansen, KJ Tingey, BT Nave, CL Wang, K Hartil, CJ Petry, AJ Buckley, L Mosthaf-Seedorf: Early growth restriction leads to down regulation of protein kinase C zeta and insulin resistance in skeletal muscle. J Endocrinol177 (2003) 235Search in Google Scholar

30 Pladys P, I Lahaie, G Cambonie, G Thibault, NL Le, D Abran, AM Nuyt: Role of brain and peripheral angiotensin II in hypertension and altered arterial baroreflex programmed during fetal life in rat. Pediatr Res55 (2004) 1042Search in Google Scholar

31 Pladys P, F Sennlaub, S Brault, D Checchin, I Lahaie, NL Le, K Bibeau, G Cambonie, D Abran, M Brochu, G Thibault, P Hardy, S Chemtob, AM Nuyt: Microvascular rarefaction and decreased angiogenesis in rats with fetal programming of hypertension associated with exposure to a low protein diet in utero. Am J Physiol Regul Integr Comp Physiol (2005)10.1152/ajpregu.00031.2005Search in Google Scholar PubMed

32 Poore KR, AJ Forhead, DS Gardner, DA Giussani, AL Fowden: The effects of birth weight on basal cardiovascular function in pigs at 3 months of age. J Physiol539 (2002) 969Search in Google Scholar

33 Poore KR, AL Fowden: The effect of birth weight on hypothalamo-pituitary-adrenal axis function in juvenile and adult pigs. J Physiol547 (2003) 107Search in Google Scholar

34 Poore KR, AL Fowden: Insulin sensitivity in juvenile and adult Large White pigs of low and high birthweight. Diabetologia47 (2004) 340Search in Google Scholar

35 Prakash YS, M Fournier, GC Sieck: Effects of prenatal undernutrition on developing rat diaphragm. J Appl Physiol75 (1993) 1044Search in Google Scholar

36 Song KS, Z Tang, S Li, MP Lisanti: Mutational analysis of the properties of caveolin-1. A novel role for the C-terminal domain in mediating homo-typic caveolin-caveolin interactions. J Biol Chem272 (1997) 4398Search in Google Scholar

37 Thompson CH, AL Sanderson, D Sandeman, C Stein, A Borthwick, GK Radda, DI Phillips: Fetal growth and insulin resistance in adult life: role of skeletal muscle morphology. Clin Sci (Lond)92 (1997) 291Search in Google Scholar

38 Walter B, R Bauer, E Gaser, U Zwiener: Validation of the multiple colored microsphere technique for regional blood flow measurements in newborn piglets. Basic Res Cardiol92 (1997) 191Search in Google Scholar

39 Wank V, R Bauer, B Walter, H Kluge, MS Fischer, R Blickhan, U Zwiener: Accelerated contractile function and improved fatigue resistance of calf muscles in newborn piglets with IUGR. Am J Physiol Regul Integr Comp Physiol278 (2000) R30410.1152/ajpregu.2000.278.2.R304Search in Google Scholar PubMed

40 Ward SS, NC Stickland: Why are slow and fast muscles differentially affected during prenatal undernutrition? Muscle Nerve14 (1991) 259Search in Google Scholar

Published Online: 2006-04-07
Published in Print: 2006-05-01

©2006 by Walter de Gruyter Berlin New York

Downloaded on 2.6.2024 from https://www.degruyter.com/document/doi/10.1515/JPM.2006.042/html
Scroll to top button