Does intrauterine crowding affect the force generating capacity and muscle composition of the piglet front limb?

English version

Autoři: Charlotte Vanden Hole ^aff001; Chris Van Ginneken ^aff001; Sara Prims ^aff001; Miriam Ayuso ^aff001; Steven Van Cruchten ^aff001; Peter Aerts ^aff002
Působiště autorů: Laboratory of Applied Veterinary Morphology, Department of Veterinary Sciences, Faculty of Biomedical, Pharmaceutical and Veterinary Sciences, University of Antwerp, Wilrijk, Belgium ^aff001; Laboratory of Functional Morphology, Department of Biology, Faculty of Sciences, University of Antwerp, Wilrijk, Belgium ^aff002; Department of Movement and Sports Sciences, Faculty of Medicine and Health Sciences, University of Ghent, Ghent, Belgium ^aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223851

Souhrn

In the pig, intrauterine competition (IUC) greatly affects postnatal traits, such as birth weight, but also locomotor capacities. In a previous study, our group discovered a lower motor performance in piglets with a low birth weight and low vitality (L piglets), compared to piglets with a normal birth weight and normal vitality (N piglets). In order to explain the force deficit causing this reduced motor performance, in a subsequent study, we investigated whether this deficit in L piglets was caused by a lower force generating capacity (FGC) of the extensors of the hind limb and/or a lower number of type II (fast-twitch) fibers in m. vastus lateralis. L piglets had a lower absolute FGC, but surprisingly, a higher relative FGC (to birth weight) in the hind limb, compared to N piglets. In addition, we found no differences in fiber composition of m. vastus lateralis. In the present study, we assessed whether this higher relative FGC is a common feature for front and hind limb locomotor muscles of L piglets. To that end, the physiological cross-sectional area of the main extensor muscles of the front limb was calculated from their volume and fiber length, in order to calculate both the absolute and the relative FGC. By immunohistochemical staining of m. triceps brachii caput longum, the percentage of type II (fast-contracting) fibers could be determined. Similar to the results of the hind limb, we found a smaller absolute FGC, but a larger relative FGC in the front limb of L piglets, compared to N piglets. In addition, m. triceps brachii caput longum did not have a different muscle fiber composition in L and N piglets. As such, we can conclude that IUC affects the locomotor muscles in the front and hind limb in a similar way and that the observed force deficit in L piglets cannot be explained by a different force generating capacity or a lower percentage of type II muscle fibers.

Klíčová slova:

Birth weight – Body limbs – Legs – Swine – Muscle fibers – Fast-twitch muscle fibers – Triceps – Slow-twitch muscle fibers

Zdroje

1. Perry J, Rowell J. Variations in foetal weight and vascular supply along the uterine horn of the pig. Journal of reproduction and fertility. 1969;19(3):527–34. doi: 10.1530/jrf.0.0190527 5809469

2. Dziuk P. Effect of migration, distribution and spacing of pig embryos on pregnancy and fetal survival. Journal of reproduction and fertility Supplement. 1985;33:57–63.

3. Fraser D. Behavioural perspectives on piglet survival. Journal of reproduction and fertility Supplement. 1990;40:355–70. 2192051

4. Wise T, Roberts A, Christenson R. Relationships of light and heavy fetuses to uterine position, placental weight, gestational age, and fetal cholesterol concentrations. Journal of animal science. 1997;75(8):2197–207. doi: 10.2527/1997.7582197x 9263069

5. Rehfeldt C, Kuhn G. Consequences of birth weight for postnatal growth performance and carcass quality in pigs as related to myogenesis. Journal of animal science. 2006;84(13_suppl):E113–E23.

6. Quiniou N, Dagorn J, Gaudré D. Variation of piglets’ birth weight and consequences on subsequent performance. Livestock Production Science. 2002;78(1):63–70.

7. Bérard J, Kreuzer M, Bee G. Effect of litter size and birth weight on growth, carcass and pork quality, and their relationship to postmortem proteolysis. Journal of Animal Science. 2008;86(9):2357–68. doi: 10.2527/jas.2008-0893 18469061

8. Alvarenga A, Chiarini-Garcia H, Cardeal P, Moreira L, Foxcroft G, Fontes D, et al. Intra-uterine growth retardation affects birthweight and postnatal development in pigs, impairing muscle accretion, duodenal mucosa morphology and carcass traits. Reproduction, Fertility and Development. 2013;25(2):387–95.

9. Bauer R, Walter B, Hoppe A, Gaser E, Lampe V, Kauf E, et al. Body weight distribution and organ size in newborn swine (sus scrofa domestica)—a study describing an animal model for asymmetrical intrauterine growth retardation. Experimental and Toxicologic Pathology. 1998;50(1):59–65. doi: 10.1016/S0940-2993(98)80071-7 9570503

10. Maltin CA, Delday MI, Sinclair KD, Steven J, Sneddon AA. Impact of manipulations of myogenesis in utero on the performance of adult skeletal muscle. Reproduction. 2001;122(3):359–74. 11597302

11. Bérard J, Pardo C, Béthaz S, Kreuzer M, Bee G. Intrauterine crowding decreases average birth weight and affects muscle fiber hyperplasia in piglets. Journal of animal science. 2010;88(10):3242–50. doi: 10.2527/jas.2010-2867 20562364

12. Vanden Hole C, Aerts P, Prims S, Ayuso M, Van Cruchten S, Van Ginneken C. Does intrauterine crowding affect locomotor development? A comparative study of motor performance, neuromotor maturation and gait variability among piglets that differ in birth weight and vitality. PloS one. 2018;13(4):e0195961. doi: 10.1371/journal.pone.0195961 29689084

13. Biewener AA. Animal locomotion: Oxford University Press; 2003.

14. Vanden Hole C, Cleuren S, Van Ginneken C, Prims S, Ayuso M, Van Cruchten S, et al. How does intrauterine crowding affect locomotor performance in newborn pigs? A study of force generating capacity and muscle composition of the hind limb. PloS one. 2018;13(12):e0209233. doi: 10.1371/journal.pone.0209233 30550550

15. Heglund NC, Cavagna GA, Taylor CR. Energetics and mechanics of terrestrial locomotion. III. Energy changes of the centre of mass as a function of speed and body size in birds and mammals. Journal of Experimental Biology. 1982;97(1):41–56.

16. Cavagna GA, Heglund NC, Taylor CR. Mechanical work in terrestrial locomotion: two basic mechanisms for minimizing energy expenditure. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 1977;233(5):R243–R61.

17. Gregersen CS, Silverton NA, Carrier DR. External work and potential for elastic storage at the limb joints of running dogs. Journal of Experimental Biology. 1998;201(23):3197–210.

18. Merkens H, Schamhardt H, OSCH GJ, Bogert Avd. Ground reaction force patterns of Dutch Warmblood horses at normal trot. Equine veterinary journal. 1993;25(2):134–7. doi: 10.1111/j.2042-3306.1993.tb02923.x 8467772

19. Witte T, Knill K, Wilson A. Determination of peak vertical ground reaction force from duty factor in the horse (Equus caballus). Journal of Experimental Biology. 2004;207(21):3639–48.

20. Alexander R, Jayes A. A dynamic similarity hypothesis for the gaits of quadrupedal mammals. Journal of zoology. 1983;201(1):135–52.

21. Alexander RM, Jayes AS. Vertical movements in walking and running. Journal of Zoology. 1978;185(MAY):27–40.

22. Merkens H, Schamhardt H. Evaluation of equine locomotion during different degrees of experimentally induced lameness I: lameness model and quantification of ground reaction force patterns of the limbs. Equine Veterinary Journal. 1988;20:99–106.

23. Shahar R, Milgram J. Morphometric and anatomic study of the forelimb of the dog. Journal of morphology. 2005;263(1):107–17. doi: 10.1002/jmor.10295 15562505

24. Schiaffino S, Reggiani C. Fiber types in mammalian skeletal muscles. Physiological reviews. 2011;91(4):1447–531. doi: 10.1152/physrev.00031.2010 22013216

25. Vanden Hole C, Goyens J, Prims S, Fransen E, Hernando MA, Van Cruchten S, et al. How innate is locomotion in precocial animals? A study on the early development of spatio-temporal gait variables and gait symmetry in piglets. Journal of Experimental Biology. 2017;220(15):2706–16.

26. Payne R, Crompton R, Isler K, Savage R, Vereecke E, Günther M, et al. Morphological analysis of the hindlimb in apes and humans. II. Moment arms. Journal of anatomy. 2006;208(6):725–42. doi: 10.1111/j.1469-7580.2006.00564.x 16761974

27. Bauer R, Wank V, Walter B, Blickhan R, Zwiener U. Reduced muscle vascular resistance in intrauterine growth restricted newborn piglets. Experimental and Toxicologic Pathology. 2000;52(3):271–6. doi: 10.1016/S0940-2993(00)80045-7 10930129

28. Wank V, Bauer R, Walter B, Kluge H, Fischer MS, Blickhan R, et al. Accelerated contractile function and improved fatigue resistance of calf muscles in newborn piglets with IUGR. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology. 2000;278(2):R304–R10. doi: 10.1152/ajpregu.2000.278.2.R304 10666129

29. Barone R. [Comparative anatomy of domestic mammals. Tome 2: Arthrology and myology].[French]1980.

30. Payne R, Hutchinson J, Robilliard J, Smith N, Wilson A. Functional specialisation of pelvic limb anatomy in horses (Equus caballus). Journal of Anatomy. 2005;206(6):557–74. doi: 10.1111/j.1469-7580.2005.00420.x 15960766

31. Hudson PE, Corr SA, Payne‐Davis RC, Clancy SN, Lane E, Wilson AM. Functional anatomy of the cheetah (Acinonyx jubatus) forelimb. Journal of Anatomy. 2011;218(4):375–85. doi: 10.1111/j.1469-7580.2011.01344.x 21332715

32. Hudson PE, Corr SA, Payne‐Davis RC, Clancy SN, Lane E, Wilson AM. Functional anatomy of the cheetah (Acinonyx jubatus) hindlimb. Journal of anatomy. 2011;218(4):363–74. doi: 10.1111/j.1469-7580.2010.01310.x 21062282

33. Williams S, Payne R, Wilson A. Functional specialisation of the pelvic limb of the hare (Lepus europeus). Journal of Anatomy. 2007;210(4):472–90. doi: 10.1111/j.1469-7580.2007.00704.x 17362487

34. Williams S, Wilson A, Payne R. Functional specialisation of the thoracic limb of the hare (Lepus europeus). Journal of anatomy. 2007;210(4):491–505. doi: 10.1111/j.1469-7580.2007.00703.x 17428206

35. Rehfeldt C, Henning M, Fiedler I. Consequences of pig domestication for skeletal muscle growth and cellularity. Livestock Science. 2008;116(1–3):30–41.

36. Gondret F, Lefaucheur L, Juin H, Louveau I, Lebret B. Low birth weight is associated with enlarged muscle fiber area and impaired meat tenderness of the longissimus muscle in pigs. Journal of Animal Science. 2006;84(1):93–103. doi: 10.2527/2006.84193x 16361495

37. Bauer R, Gedrange T, Bauer K, Walter B. Intrauterine growth restriction induces increased capillary density and accelerated type I fiber maturation in newborn pig skeletal muscles. Journal of perinatal medicine. 2006;34(3):235–42. doi: 10.1515/JPM.2006.042 16602845

38. Lefaucheur L, Hoffman R, Gerrard D, Okamura C, Rubinstein N, Kelly A. Evidence for three adult fast myosin heavy chain isoforms in type II skeletal muscle fibers in pigs. Journal of animal science. 1998;76(6):1584–93. doi: 10.2527/1998.7661584x 9655578

39. Larsson L, Edstrom L, Lindegren B, Gorza L, Schiaffino S. MHC composition and enzyme-histochemical and physiological properties of a novel fast-twitch motor unit type. American Journal of Physiology-Cell Physiology. 1991;261(1):C93–C101.

40. Eddinger TJ, Moss RL. Mechanical properties of skinned single fibers of identified types from rat diaphragm. American Journal of Physiology-Cell Physiology. 1987;253(2):C210–C8.

41. Sieck GC, Han Y-S, Prakash Y, Jones KA. Cross-bridge cycling kinetics, actomyosin ATPase activity and myosin heavy chain isoforms in skeletal and smooth respiratory muscles1. Comparative Biochemistry and Physiology Part B: Biochemistry and Molecular Biology. 1998;119(3):435–50.

42. Staun H. Various factors affecting number and size of muscle fibers in the pig. Acta Agriculturae Scandinavica. 1963;13(3):293–322.

43. Stickland N, Goldspink G. A possible indicator muscle for the fibre content and growth characteristics of porcine muscle. Animal Science. 1973;16(2):135–46.

44. Miller L, Garwood V, Judge M. Factors affecting porcine muscle fiber type, diameter and number. Journal of Animal Science. 1975;41(1):66–77.

45. Dwyer C, Fletcher J, Stickland N. Muscle cellularity and postnatal growth in the pig. Journal of Animal Science. 1993;71(12):3339–43. doi: 10.2527/1993.71123339x 8294285

46. Suzuki A, Cassens R. A Histochemical Study of Myofiber Types in Muscle of the Growing Pig 1. Journal of Animal Science. 1980;51(6):1449–61. doi: 10.2527/jas1981.5161449x 6451606

47. Lefaucheur L, Vigneron P. Post-natal changes in some histochemical and enzymatic characteristics of three pig muscles. Meat science. 1986;16(3):199–216. doi: 10.1016/0309-1740(86)90026-4 22054929

48. Fazarinc G, Bavdek S, Lorger J. Postnatal histochemical and morphometric changes in the muscles of the domestic pig. Zb Vet Fak Univ Ljubljana. 1991;28:151–65.

49. Handel S, Stickland N. The growth and differentiation of porcine skeletal muscle fibre types and the influence of birthweight. Journal of anatomy. 1987;152:107. 2958439

50. Lefaucheur L. Myofiber typing and pig meat production. Slovenian veterinary research. 2001;38(1):5–28.

51. Wigmore P, Stickland N. Muscle development in large and small pig fetuses. Journal of Anatomy. 1983;137(Pt 2):235.

52. Ono Y, Solomon M, Evock-Clover C, Steele N, Maruyama K. Effects of porcine somatotropin administration on porcine muscles located within different regions of the body. Journal of animal science. 1995;73(8):2282–8. doi: 10.2527/1995.7382282x 8567464

53. Solomon M, Caperna T, Mroz R, Steele NJJoas. Influence of dietary protein and recombinant porcine somatotropin administration in young pigs: III. Muscle fiber morphology and shear force. 1994;72(3):615–21.

54. Elder G, Bradbury K, Roberts RJJoAP. Variability of fiber type distributions within human muscles. 1982;53(6):1473–80.

55. Henckel P, editor Properties of muscle fibre types as a source of variation in meat quality. Proceedings of the 19th World’s Poultry Congress, Amsterdam, The Netherlands; 1992.

Does intrauterine crowding affect the force generating capacity and muscle composition of the piglet front limb?

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