Skip to main content
SpringerLink
Log in

Mechanical properties of the porcine growth plate vary with developmental stage

  • Original Paper
  • Published:
Biomechanics and Modeling in Mechanobiology Aims and scope Submit manuscript

Abstract

The objectives of this study were to extract the intrinsic mechanical properties of the growth plate at four different stages of growth and to compare two different methods of extracting these properties. Porcine distal ulnar growth plate samples were obtained from newborn, 4-, 8-, and 18-week (W) pigs and were tested using stress relaxation tests under unconfined compression. A four-parameter curve fitting procedure was developed to extract mechanical properties using the Transversely Isotropic Biphasic Elastic model(TIBPE) (Cohen et al. in J Biomech Eng Trans Asme 120(4):491–496, 1998) and the Differential Evolution (DE) optimization algorithm (Price et al. Natural computing series, Springer, Germany 2005). Optimization was done on all experimental curves for the first method and on one average experimental curve per developmental stage in the second. The 4-week stage was studied in two subgroups (a) and (b) due to distinct differences in mechanical properties. Intrinsic mechanical properties of the growth plate varied nonlinearly with developmental stage. Both methods showed that transverse and out-of-plane Young’s moduli (E 1, E 3) decrease with developmental stage, whereas transverse permeability (k 1) increases. The exception is a sharp increase in stiffness and reduction in permeability at the 4W(a) stage, which may be associated with rapid porcine developmental changes at the 3–4 week period. The second method provides a more reliable representation of the average mechanical behavior, whereas the first method allows statistical comparison of optimized mechanical properties. This study characterizes, for the first time, the variation in growth plate mechanical properties for the same animal (porcine) and bone (ulna) model with developmental stage and provides new insight into the progression of musculoskeletal diseases during growth spurts in response to mechanical loading.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Abbreviations

E 1 :

Transverse Young’s modulus

E 3 :

Out-of-plane Young’s modulus

k 1 :

Transverse permeability

ν 21 :

Transverse Poisson’s ratio

ν 31 :

Out-of-plane Poisson’s ratio

References

  • Alexander CJ (1976) Effect of growth rate of strength of the growth plate-shaft junction. Skeletal Radiol 1: 67–76

    Article  Google Scholar 

  • Ballock R, O’Keefe R (2003) Physiology and pathophysiology of the growth plate. Birth Defects Res 69: 123–143

    Article  Google Scholar 

  • Bonnel F, Dimeglio A, Baldet P, Rabischong P (1984) Biomechanical activity of the growth plate. Rev Clin Anat 6: 53–61

    Article  Google Scholar 

  • Bursac PM, Obitz TW, Eisenberg SR, Stamenovic D (1999) Confined and unconfined stress relaxation of cartilage: appropriateness of a transversely isotropic analysis. J Biomech 32: 1125–1130

    Article  Google Scholar 

  • Chagin AS, Savendahl L (2007) Oestrogen receptors and linear bone growth. Acta Pædiatrica 96: 1275–1279

    Article  Google Scholar 

  • Cohen B, Chorney GS, Phillips DP, Dick HM, Mow VC (1994) Compressive stress-relaxation behavior of bovine growth-plate may be described by the nonlinear biphasic theory. J Orthop Res 12(6): 804–813

    Article  Google Scholar 

  • Cohen B, Lai WM, Mow VC (1998) A transversely isotropic biphasic model for unconfined compression of growth plate and chondroepiphysis. J Biomech Eng Trans Asme 120(4): 491–496

    Article  Google Scholar 

  • Corson AM, Laws J, Laws A, Litten JC, Lean IJ, Clarke L (2008) Percentile growth charts for biomedical studies using a porcine model. Animal 2(12): 1795–1801

    Article  Google Scholar 

  • Davies AS, Tan Y, Broad TE (1984) Growth gradients in the skeleton of cattle, sheep and pigs. Vet Med C Anat Histol Embryol 13: 222–230

    Article  Google Scholar 

  • Dickson RA (1983) Scolisos in the community. Br Med J 286: 615–619

    Article  Google Scholar 

  • Disilvestro MR, Zhu QL, Wong M, Jurvelin JS, Suh JKF (2001) Biphasic poroviscoelastic simulation of the unconfined compression of articular cartilage: I. Simultaneous prediction of reaction force and lateral displacement. J Biomech Eng Trans Asme 123(2): 191–197

    Article  Google Scholar 

  • Duval-Beaupère G (1971) Pathogenic relationship between scoliosis and growth. In: Scoliosis and growth, proceedings of the third symposium, Churchill Livingstone, Edinburgh, pp 58–64

  • Farnum CE, Wilsman NJ (1998) Growth plate cellular function. In: Buckwalterea JA (eds) Skeletal morphogenesis and growth. American Academy of Orthopaedic Surgeons, Rosemont, pp 203–224

    Google Scholar 

  • Fortin MSJ, Shirazi-Adl A, Hunziker EB, Buschmann MD (2000) Unconfined compression of articular cartilage: nonlinear behavior and comparison with a fibril-reinforced biphasic model. J Biomech Eng 122: 189–195

    Article  Google Scholar 

  • França LR, Silva VA, Chiarini-Garcia H, Garcia SK, Debeljuk L (2000) Cell proliferation and hormonal changes during postnatal development of the testis in the pig. Biol Reprod 63: 1629–1636

    Article  Google Scholar 

  • Gupta S, Lin J, Ashby P, Pruitt L (2009) A fiber reinforced poroelastic model of nanoindentation of porcine costal cartilage: A combined experimental and finite element approach. J Mech Behav Biomed Mater 2: 326–338

    Article  Google Scholar 

  • Hunziker EB, Schenk RK (1989) Physiological mechanisms adopted by chondrocytes in regulating longitudinal bone growth in rats. J Physiol 414: 55–71

    Google Scholar 

  • Irie T, Aizawa T, Kokobun S (2005) The role of sex hormones in the kinetics of chondrocytes in the growth plate: a study in the rabbit. J Bone Joint Surg [Br] 87: 1278–1284

    Google Scholar 

  • Isaksson HD, van Corrinus C, Ito K (2009) Sensitivity of tissue differentiation and bone healing prediction to tissue properties. J Biomech 42: 555–564

    Article  Google Scholar 

  • Juul A (2001) The effect of oestrogens on linear bone growth. Human Reprod Update 7(3): 303–313

    Article  Google Scholar 

  • Kajee-Bagdadi Z (2007) Constrained global optimization. Master’s Thesis, University of the Witwatersrand, Johannesburg

  • Kelley CT (1999) Iterative methods for optimization. In: Mathematics sfiaa (ed)

  • Lempriere BM (1968) Poisson’s ratio in orthotropic materials. AIAA J 6(11): 2226–2227

    Article  Google Scholar 

  • Leveau B, Bernhardt D (1984) Developmental biomechanics—effect of forces on the growth, development, and maintenance of the human body. Phys Therapy 64(12): 1874–1882

    Google Scholar 

  • Lu XL, Sun DDN, Guo XE, Chen FH, Lai WM, Mow VC (2004) Indentation determined mechanoelectrochemical properties and fixed charge density of articular cartilage. Ann Biomed Eng 32(3): 370–379

    Article  Google Scholar 

  • Mansour JM, Mow VC (1976) The permeability of articular cartilage under compressive strain and at high pressures. J Bone Joint Surg 58: 509–516

    Google Scholar 

  • Maor G, Segev Y, Phillip M (1999) Testosterone stimulates insulin-like growth factor-I and insulin-like growth factor-I-receptor gene expression in the mandibular condyle—a model of endochondral ossification. Endocrinology 140: 1901–1910. doi:10.1210/en.140.4.1901

    Article  Google Scholar 

  • Mehlman CT, Koepplinger ME (2010) Growth plate (physeal) fractures. Emedicine—webmd

  • Morais T, Bernier M, Turcotte F (1985) Age and sex specific prevalence of scoliosis and the value of school screening programs. Am J Public Health 75: 1377–1380

    Article  Google Scholar 

  • Mow VCKSC, Lai WM, Armstrong CG (1980) Biphasic creep and stress relaxation of articular cartilage in compression: theory and experiments. J Biomech Eng 102: 73–84

    Article  Google Scholar 

  • Peralta JM, Arnold AM, Currie WB, Thonney ML (1994) Effects of testosterone on skeletal growth in lambs as assessed by labeling index of chondrocytes in the metacarpal bone growth plate. J Animal Sci 72: 2629–2634

    Google Scholar 

  • Phillip M, Maor G, Assa S, Silbergeld A, Segev Y (2001) Testosterone stimulates growth of tibial epiphyseal growth plate and insulin-like growth factor-1 receptor abundance in hypophysectomized and castrated rats. Endocrine 16(1): 1–6

    Article  Google Scholar 

  • Price K, Storn RM, Lampinen JA (2005) Differential evolution: a practical approach to global optimization. Natural computing series. Springer, Germany

    Google Scholar 

  • Radhakrishnan PLN, Mao JJ (2004) Zone-specific micromechanical properties of the extracellular matrices of growth plate cartilage. Ann Biomed Eng 32(2): 284–291

    Article  Google Scholar 

  • Rauch F (2005) Bone growth in length and width: the Yin and Yang of bone stability. J Musculoskelet Neuronal Interact 5(3): 194–201

    Google Scholar 

  • Reynaud BQ, Thomas M (2006) Anisotropic hydraulic permeability in compressed articular cartilage. J Biomech 39: 131–137

    Article  Google Scholar 

  • Savendahl L (2005) Hormonal regulation of growth plate cartilage. Hormone Res 64: 94–97

    Article  Google Scholar 

  • Sergerie K, Lacoursière M, Villemure I, Lévesque M (2009) Mechanical properties of the porcine growth plate and its three zones from unconfined compression tests. J Biomech 42: 510–516

    Article  Google Scholar 

  • Soucacos PN, Soucacos PK, Zacharis KC, Beris AE, Xenakis TA (1997) School-screening for scoliosis. A prospective epidemiological study in northwestern and Central Greece. J Bone Joint Surg Am 79: 1498–1503

    Google Scholar 

  • Stokes IAF, Clark KC, Farnum CE, Aronsson DD (2007) Alterations in the growth plate associated with growth modulation by sustained compression or distraction. Bone 41(2): 197–205. doi:10.1016/j.bone.2007.04.180

    Article  Google Scholar 

  • Tanck E, Hannink G, Ruimerman R, Buma P, Burger EH, Huiskes R (2006) Cortical bone development under the growth plate is regulated by mechanical load transfer. J Anat 208(1): 73–79

    Article  Google Scholar 

  • Trudeau VL, Meijer JC, Erkens JHF, van de Wiel DFM, Wensing CJG (1992) Pubertal development in the male pig: effects of treatment with a long-acting gonadotropin-releasing hormone agonist on plasma luteinizing hormone, follicle stimulating hormone and testosterone. Can J Vet Res 56: 102–109

    Google Scholar 

  • Van der Eerden BCJ, Van de Ven J, Lowik CWGM, Wit JM, Karperien M (2002) Sex steroid metabolism in the tibial growth plate of the rat. Endocrinology 143: 4055–4948

    Article  Google Scholar 

  • Vander Eerden BKM, Wit JM (2003) Systemic and local regulation of the growth plate. Endocr Rev 24(6): 782–801

    Article  Google Scholar 

  • Villemure I, Chung MAL, Matyas JR, Duncan NA (2004) Mechanical properties of rat cartilaginous growth plates vary with developmental stages. In: Sawatzky BJ (ed) International Research Society of Spinal Deformities

  • Villemure I, Cloutier L, Matyas JR, Duncan NA (2007) Non-uniform strain distribution within rat cartilaginous growth plate under uniaxial compression. J Biomech 40(1): 149–156

    Article  Google Scholar 

  • Williamson AK, Chen AC, Sah RL (2001) Compressive properties and function-composition relationships of developing bovine articular cartilage. J Orthop Res 19: 1113–1121

    Article  Google Scholar 

  • Wilsman NJ, Farnum CE, Leiferman EM, Fry M, Barreto C (1996) Differential growth by growth plate kinetics as a function of multiple parameters of chondrocyte kinetics. J Orthop Res 14: 927–936

    Article  Google Scholar 

  • Wong M, Ponticiello M, Kovanen V, Jurvelin JS (2000) Volumetric changes of articular cartilage during stress relaxation in unconfined compression. J Biomech 33: 1049–1054

    Article  Google Scholar 

  • Yawn BP, Yawn RA, Hodge D, Kurland M, Shaughnessy WJ, Ilstrup D, Jacobsen SJ (1999) A population-based study of school scoliosis screening. JAMA 282: 1427–1432

    Article  Google Scholar 

  • Ylikoski M (1993) Spinal growth and progression of adolescent idiopathic scoliosis. Eur Spine J 1: 236–239

    Article  Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Mechanical Engineering, École Polytechnique de Montréal, P.O. Box 6079, Station Centre-Ville, Montréal, QC, H3C 3A7, Canada

    Roxanne Wosu, Kim Sergerie & Isabelle Villemure

  2. CHU Sainte-Justine Research Center, 3175 Côte-Ste-Catherine Rd., Montréal, QC, H3T 1C5, Canada

    Kim Sergerie & Isabelle Villemure

  3. Center for Applied Research on Polymers and Composites, École Polytechnique de Montréal, P.O. Box 6079, Station Centre-Ville, Montréal, QC, H3C 3A7, Canada

    Martin Lévesque

Authors
  1. Roxanne Wosu
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Kim Sergerie
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Martin Lévesque
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Isabelle Villemure
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Isabelle Villemure.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Wosu, R., Sergerie, K., Lévesque, M. et al. Mechanical properties of the porcine growth plate vary with developmental stage. Biomech Model Mechanobiol 11, 303–312 (2012). https://doi.org/10.1007/s10237-011-0310-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10237-011-0310-6

Keywords

Search

Navigation