Enhanced femoral neck strength in response to weightlifting exercise training in maturing male rats

International SportMed Journal

Volumn 14, Issue 3, 2013, Pages 155-167

  Drummond, Lucas Rios ^a   Del Carlo, Ricardo Junqueira ^a   Melo, Stéphano Freitas Soares ^b   Carneiro, Miguel Araújo ^c   Da Silva, Karina Ana ^a   Rodrigues, Aurora Corrêa ^a   Soares, Pedro Natali Pinheiro ^a   Gomes, Thales Nicolau Prímola ^a   Lousada, Mário Jefferson Quirino ^d   De Oliveira, Edilamar Menezes ^b   Natali, Antônio José ^a  

^a FEDERAL UNIVERSITY OF VIÇOSA   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c FEDERAL UNIVERSITY OF ESPÍRITO SANTO   (Brazil)

^d NONE

Author keywords

Bone mass; Collagen type III; Hip fracture; Physical activity; Resistance exercise

Indexed keywords

EID: 84885053101     PISSN: None     EISSN: 15283356     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Gennari L, Bilezikian JP. Osteoporosis in men. Endocrinol Metab Clin N Am. 2007; 36: 399-419
2. Campion JM, Maricic MJ. Osteoporosis in men. American Family Physician. 2003; 67(7):1521-1526.
3. Thorngren KG, Hommel A, Norrman PO, et al. Epidemiology of femoral neck fractures. Injury. 2002 Dec;33 (Suppl 3):C1-7
4. Bagi CM, Wilkie D, Georgelos K, et al. Morphological and structural characteristics of the proximal femur in human and rat. Bone. 1997 Sep;21(3):261-267
5. Rybicki EF, Simonen FA, Weis EB, Jr. On the mathematical analysis of stress in the human femur. J Biomech. 1972 Mar;5(2):203-215.
6. Crawford AJ, Hamblen DL. Thigh and knee: Outline of fractures. Edinburgh: Churchill Livingstone; 1992. p. 190-226
7. Luther F, Saino H, Carter DH, et al. Evidence for an extensive collagen type III/VI proximal domain in the rat femur. I. Diminution with ovariectomy. Bone 2003 Jun;32(6):652-659.
8. Knott L, Bailey AJ. Collagen cross-links in mineralizing tissues: a review of their chemistry, function, and clinical relevance. Bone 1998 Mar;22(3):181-187
9. Banse X, Devogelaer JP, Lafosse A, et al. Cross-link profile of bone collagen correlates with structural organization of trabeculae. Bone 2002 Jul;31(1):70-76
10. Holopainen JT, Brama PA, Halmesmaki E, et al. Changes in subchondral bone mineral density and collagen matrix organization in growing horses. Bone. 2008 Dec;43(6):1108-1114
11. Wang X, Shen X, Li X, Agrawal CM. Age-related changes in the collagen network and toughness of bone. Bone 2002 Jul;31(1):1-7
12. Kohn DH, Sahar ND, Wallace JM, et al. Exercise alters mineral and matrix composition in the absence of adding new bone. Cells Tissues Organs 2008;189(1-4):33-37
13. Brama PA, Bank RA, Tekoppele JM, et al. Training affects the collagen framework of subchondral bone in foals. Vet J 2001 Jul;162(1):24-32
14. Brama PA, TeKoppele JM, Bank RA, et al. Biochemical development of subchondral bone from birth until age eleven months and the influence of physical activity. Equine Vet J 2002 Mar;34(2):143-149
15. Saino H, Luther F, Carter DH, et al. Evidence for an extensive collagen type III proximal domain in the rat femur. II. Expansion with exercise. Bone 2003 Jun;32(6):660-668
16. Isaksson H, Tolvanen V, Finnila MA, et al. Long-term voluntary exercise of male mice induces more beneficial effects on cancellous and cortical bone than on the collagenous matrix. Exp Gerontol 2009 Nov;44(11):708-717
17. Kukuljan S, Nowson CA, Bass SL, et al. Effects of a multi-component exercise program and calcium-vitamin-D3-fortified milk on bone mineral density in older men: A randomised controlled trial. Osteoporos Int 2009 Mar; 20(7):1241-1251.
18. Bono CM, Einhorn TA. Overview of osteoporosis: pathophysiology and determinants of bone strength. Eur Spine J 2003 Oct;12 (Suppl 2):S90-96.
19. Henry YM, Fatayerji D, Eastell R. Attainment of peak bone mass at the lumbar spine, femoral neck and radius in men and women: Relative contributions of bone size and volumetric bone mineral density. Osteoporos Int 2004 Apr; 15(4):263-273.
20. Blanchet C, Chagnon CLeA, Thibault G. Activité physique et santé osseuse. In: Ministère de l'Éducation dLedS, gouvernement du Québec, ed. Quebec: Comité scientifique de Kino-Québec; 2008. p. 40
21. Brahm H, Strom H, Piehl-Aulin K, et al. Bone metabolism in endurance trained athletes: A comparison to population-based controls based on DXA, SXA, quantitative ultrasound, and biochemical markers. Calcif Tissue Int 1997 Dec;61(6):448-454.
22. Iwamoto J, Shimamura C, Takeda T, et al. Effects of treadmill exercise on bone mass, bone metabolism, and calciotropic hormones in young growing rats. J Bone Miner Metab 2004 Sep;22(1):26-31.
23. Huang TH, Chang FL, Lin SC, et al. Endurance treadmill running training benefits the biomaterial quality of bone in growing male Wistar rats. J Bone Miner Metab 2008 Aug;26(4):350-357.
24. Huang TH, Hsieh SS, Liu SH, et al. Swimming training increases the post-yield energy of bone in young male rats. Calcif Tissue Int 2010 Feb;86(2):142-153
25. Fujimura R, Ashizawa N, Watanabe M, et al. Effect of resistance exercise training on bone formation and resorption in young male subjects assessed by biomarkers of bone metabolism. J Bone Miner Res 1997 Feb; 12 (4): 656-662.
26. Notomi T, Lee SJ, Okimoto N, et al. Effects of resistance exercise training on mass, strength, and turnover of bone in growing rats. Eur J Appl Physiol 2000 Jul;82(4):268-274.
27. Notomi T, Okazaki Y, Okimoto N, et al. A comparison of resistance and aerobic training for mass, strength and turnover of bone in growing rats. Eur J Appl Physiol 2000 Dec;83(6):469-474
28. Tamaki T, Uchiyama S, Nakano S. A weight-lifting exercise model for inducing hypertrophy in the hindlimb muscles of rats. Med Sci Sports Exerc 1992 Aug; (24): 881-886
29. Pajamaki I, Sievanen H, Kannus P, et al. Skeletal effects of estrogen and mechanical loading are structurally distinct. Bone 2008 Oct;43(4):748-757
30. Shimano MM & Volpon JB. Biomechanics and structural adaptations of the rat femur after hindlimb suspension and treadmill running. Braz J Med Biol Res 2009 Apr;42(4):330-338.
31. Junqueira LCU, Cossermelli W, Brentani R. Differential staining of collagens type I, II, and III by Sirius Red and polarization microscopy. Arch Histol Jpn 1978; 41. 267-272.
32. Robling AG, Castillo AB, Turner CH. Biomechanical and molecular regulation of bone remodeling. Annu Rev Biomed Eng 2006 Jul;8:455-498.
33. Joo Y-I, Sone T, Fukunaga M, et al. Effects of endurance exercise on three-dimensional trabecular bone microarchitecture in young growing rats. Bone 2003 Oct; 33 (4), 485-493.
34. Saito M, Marumo K. Collagen cross-links as a determinant of bone quality: A possible explanation for bone fragility in aging, osteoporosis, and diabetes mellitus. Osteoporos Int 2010 Feb;21(2):195-214.
35. Puustjarvi K, Nieminen J, Rasanen T, et al. Do more highly organized collagen fibrils increase bone mechanical strength in loss of mineral density after one-year running training? J Bone Miner Res 1999 Mar;14(3):321-329
36. Burr DB. The contribution of the organic matrix to bone's material properties. Bone 2002 Jul;31(1):8-11
37. Skedros JG, Dayton MR, Sybrowsky CL, et al. The influence of collagen fiber orientation and other histocompositional characteristics on the mechanical properties of equine cortical bone. J Exp Biol 2006 Aug;209(Pt 15):3025-3042
38. Carter DH, Sloan P, Aaron JE. Immunolocalization of collagen types I and III, tenascin, and fibronectin in intramembranous bone. J Histochem Cytochem 1991 Mar; 39 (5): 599-606.
39. Kielty CM, Hopkinson I, Grant ME. The collagen family: Structure, assembly and organization in the extracellular matrix. In: Royce PM, Steinmann B, eds. Connective tissue and its heritable disorders. New York: Wiley-Liss; 1993, p. 103-147.
40. Aaron JE. Periosteal Sharpey's fibers: A novel bone matrix regulatory system? Front Endocrinol (Lausanne) 2012; 3: 98. doi: 10.3389/fendo.2012.00098.
41. Aaron JE, Skerry TM. Intramembranous trabecular generation in normal bone. Bone Miner 1994 Sep; 25: 211-230.
42. Simmons DJ, Menton DN, Miller S, et al. Periosteal attachment fibres in the rat calvarium. Calcif Tissue Int 1993 Dec;53: 424-427.
43. Vashishth D. Small animal bone biomechanics. Bone 2008 Nov;43(5):794-797.
44. Iwaniec UT, Dube MG, Boghossian S, et al. Body mass influences cortical bone mass independent of leptin signaling. Bone 2009 Mar;44(3):404-412.
45. Shuster S. Osteoporosis, a unitary hypothesis of collagen loss in skin and bone. Med Hypotheses 2005; 65(3):426-432.
46. Saito M. Poor bone quality in diabetes: Detrimental collagen cross-link pattern reduces bone strength without change in bone mineral density. Clin Calcium 2006 Aug;16(8):1287-1295.
47. Fassbender WJ, Godde M, Brandenburg VM, et al. Urinary bone resorption markers (deoxypyridinoline and C-terminal telopeptide of type I collagen) in healthy persons, postmenopausal osteoporosis and patients with type I diabetes. Adv Med Sci 2009;54(1):1-6
48. Junqueira LCU, Bignolas G, Brentani R. Picrocirius staining plus polarization microscopy: A specific method for collagen detection in tissue sections. Histochem J 1979 Jul; 11: 447-453.
49. Montes GS, Krisztan RM, Shigihara KM, et al. Histochemical and morphological characterization of reticular fibers. Histochemistry 1980 Feb; 65: 131-137.
50. Zambrano NZ, Montes GS, Shigihara KM, et al. Collagen arrangement in cartilages. Acta Anat 1982 Jul; 113: 26-32.
51. Tulberg-Reinert H, Jundt G. In situ measurement of collagen synthesis by human bone cells with Sirius Red-based colorimetric microassay: Effects of transforming growth factor β2 and ascorbic acid 2-phosphate. Histochemi Cell Biol 1999 Dec; 112: 271-276.