Reduced gravitational loading does not account for the skeletal effect of botulinum toxin-induced muscle inhibition suggesting a direct effect of muscle on bone

Bone

Volumn 54, Issue 1, 2013, Pages 98-105

  Warden, Stuart J ^a   Galley, Matthew R ^a   Richard, Jeffrey S ^a   George, Lydia A ^a   Dirks, Rachel C ^a   Guildenbecher, Elizabeth A ^a   Judd, Ashley M ^a   Robling, Alexander G ^a   Fuchs, Robyn K ^a  

^a INDIANA UNIVERSITY   (United States)

Author keywords

Botox; Mechanical loading; Muscle bone interaction; Myokines; Tail suspension

Indexed keywords

BOTULINUM TOXIN; BOTULINUM TOXIN A;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BONE MASS; BONE STRESS; BOTULINUM TOXIN INDUCED MUSCLE INHIBITION; COMPUTER ASSISTED TOMOGRAPHY; CONTROLLED STUDY; CORTICAL BONE; CORTICAL THICKNESS (BONE); DRUG INDUCED DISEASE; FEMALE; GRAVITY; HINDLIMB; MOUSE; MUSCLE ATROPHY; MUSCLE STRESS; NONHUMAN; OSTEOLYSIS; SKELETAL MUSCLE; SKELETON; TIBIA; TRABECULAR BONE;

ANIMALS; BOTULINUM TOXINS; FEMALE; GRAVITATION; HINDLIMB SUSPENSION; MICE; MICE, INBRED C57BL; MUSCLE, SKELETAL; TIBIA; WEIGHT-BEARING;

EID: 84874385602     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2013.01.043     Document Type: Article

References (39)

1. Duncan R.L., Turner C.H. Mechanotransduction and the functional response of bone to mechanical strain. Calcif Tissue Int 1995, 57:344-358.
2. Judex S., Carlson K.J. Is bone's response to mechanical signals dominated by gravitational loading?. Med Sci Sports Exerc 2009, 41:2037-2043.
3. Kohrt W.M., Barry D.W., Schwartz R.S. Muscle forces or gravity: what predominates mechanical loading on bone?. Med Sci Sports Exerc 2009, 41:2050-2055.
4. Robling A.G. Is bone's response to mechanical signals dominated by muscle forces?. Med Sci Sports Exerc 2009, 41:2044-2049.
5. Burr D.B. Muscle strength, bone mass, and age-related bone loss. J Bone Miner Res 1997, 12:1547-1551.
6. Frost H.M. On our age-related bone loss: insights from a new paradigm. J Bone Miner Res 1997, 12:1539-1546.
7. Judex S., Rubin C.T. Is bone formation induced by high-frequency mechanical signals modulated by muscle activity?. J Musculoskelet Neuronal Interact 2010, 10:3-11.
8. Donahue S.W. The role of muscular force and fatigue in stress fractures. Musculoskeletal fatigue and stress fractures 2001, 131-149. CRC Press, Bota Raton, Florida, USA. D.B. Burr, C. Milgrom (Eds.).
9. Scott S.H., Winter D.A. Internal forces at chronic running injury sites. Med Sci Sports Exerc 1990, 22:357-369.
10. Arndt A., Ekenman I., Westblad P., Lundberg A. Effects of fatigue and load variation on metatarsal deformation measured in vivo during barefoot walking. J Biomech 2002, 35:621-628.
11. Fyhrie D.P., Milgrom C., Hoshaw S.J., Simkin A., Dar S., Drumb D., et al. Effect of fatiguing exercise on longitudinal bone strain as related to stress fracture in humans. Ann Biomed Eng 1998, 26:660-665.
12. Milgrom C., Radeva-Petrova D.R., Finestone A., Nyska M., Mendelson S., Benjuya N., et al. The effect of muscle fatigue on in vivo tibial strains. J Biomech 2007, 40:845-850.
13. Sharkey N.A., Ferris L., Smith T.S., Matthews D.K. Strain and loading of the second metatarsal during heel-lift. J Bone Joint Surg Am 1995, 77:1050-1057.
14. Armstrong D.W., Rue J.-P.H., Wilckens J.H., Frassica F.J. Stress fracture injury in young military men and women. Bone 2004, 35:806-816.
15. Beck T.J., Ruff C.B., Shaffer R.A., Betsinger K., Trone D.W., Brodine S.K. Stress fracture in military recruits: gender differences in muscle and bone susceptibility factors. Bone 2000, 27:437-444.
16. Bennell K.L., Malcolm S.A., Thomas S.A., Reid S.J., Brukner P.D., Ebeling P.R., et al. Risk factors for stress fractures in track and field athletes: a twelve-month prospective study. Am J Sports Med 1996, 24:810-818.
17. Popp K.L., Hughes J.M., Smock A.J., Novotny S.A., Stovitz S.D., Koehler S.M., et al. Bone geometry, strength, and muscle size in runners with a history of stress fracture. Med Sci Sports Exerc 2009, 41:2145-2150.
18. Schnackenburg K.E., Macdonald H.M., Ferber R., Wiley J.P., Boyd S.K. Bone quality and muscle strength in female athletes with lower limb stress fractures. Med Sci Sports Exerc 2011, 43:2110-2119.
19. Aliprantis A.O., Stolina M., Kostenuik P.J., Poliachik S.L., Warner S.E., Bain S.D., et al. Transient muscle paralysis degrades bone via rapid osteoclastogenesis. FASEB J 2012, 26:1110-1118.
20. Ausk B.J., Huber P., Poliachik S.L., Bain S.D., Srinivasan S., Gross T.S. Cortical bone resorption following muscle paralysis is spatially heterogeneous. Bone 2012, 50:14-22.
21. Bouvard B., Mabilleau G., Legrand E., Audran M., Chappard D. Micro and macroarchitectural changes at the tibia after botulinum toxin injection in the growing rat. Bone 2012, 50:858-864.
22. Chappard D., Chennebault A., Moreau M., Legrand E., Audran M., Basle M.F. Texture analysis of X-ray radiographs is a more reliable descriptor of bone loss than mineral content in a rat model of localized disuse induced by the Clostridium botulinum toxin. Bone 2001, 28:72-79.
23. Grimston S.K., Goldberg D.B., Watkins M., Brodt M.D., Silva M.J., Civitelli R. Connexin43 deficiency reduces the sensitivity of cortical bone to the effects of muscle paralysis. J Bone Miner Res 2011, 26:2151-2160.
24. Grimston S.K., Silva M.J., Civitelli R. Bone loss after temporarily induced muscle paralysis by botox is not fully recovered after 12weeks. Ann N Y Acad Sci 2007, 1116:444-460.
25. Manske S.L., Boyd S.K., Zernicke R.F. Muscle changes can account for bone loss after botulinum toxin injection. Calcif Tissue Int 2010, 87:541-549.
26. Manske S.L., Boyd S.K., Zernicke R.F. Muscle and bone follow similar temporal patterns of recovery from muscle-induced disuse due to botulinum toxin injection. Bone 2010, 46:24-31.
27. Manske S.L., Boyd S.K., Zernicke R.F. Vertical ground reaction forces diminish in mice after botulinum toxin injection. J Biomech 2011, 44:637-643.
28. Manske S.L., Good C.A., Zernicke R.F., Boyd S.K. High-frequency, low-magnitude vibration does not prevent bone loss resulting from muscle disuse in mice following botulinum toxin injection. PLoS One 2012, 7:e36486.
29. Poliachik S.L., Bain S.D., Threet D., Huber P., Gross T.S. Transient muscle paralysis disrupts bone homeostasis by rapid degradation of bone morphology. Bone 2010, 46:18-23.
30. Sheng Z.F., Ma Y.L., Tong D., Fang D.Y., Liang Q.C., Liu L.H., et al. Strontium ranelate prevents bone loss in a rat model of localized muscle paralysis. Ann Biomed Eng 2012, 40:657-665.
31. Thomsen J.S., Christensen L.L., Vegger J.B., Nyengaard J.R., Bruel A. Loss of bone strength is dependent on skeletal site in disuse osteoporosis in rats. Calcif Tissue Int 2012, 90:294-306.
32. Warner S.E., Sanford D.A., Becker B.A., Bain S.D., Srinivasan S., Gross T.S. Botox induced muscle paralysis rapidly degrades bone. Bone 2006, 38:257-264.
33. Warden S.J., Hassett S.M., Bond J.L., Rydberg J., Grogg J.D., Hilles E.L., et al. Psychotropic drugs have contrasting skeletal effects that are independent of their effects on physical activity levels. Bone 2010, 46:985-992.
34. Schmidt C., Priemel M., Kohler T., Weusten A., Muller R., Amling M., et al. Precision and accuracy of peripheral quantitative computed tomography (pQCT) in the mouse skeleton compared with histology and microcomputed tomography (microCT). J Bone Miner Res 2003, 18:1486-1496.
35. Doube M., Klosowski M.M., Arganda-Carreras I., Cordelieres F.P., Dougherty R.P., Jackson J.S., et al. BoneJ: free and extensible bone image analysis in ImageJ. Bone 2010, 47:1076-1079.
36. Pedersen B.K., Febbraio M.A. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 2012, 8:457-465.
37. Elkasrawy M.N., Hamrick M.W. Myostatin (GDF-8) as a key factor linking muscle mass and bone structure. J Musculoskelet Neuronal Interact 2010, 10:56-63.
38. Hamrick M.W., McNeil P.L., Patterson S.L. Role of muscle-derived growth factors in bone formation. J Musculoskelet Neuronal Interact 2010, 10:64-70.
39. Hamrick M.W. A role for myokines in muscle-bone interactions. Exerc Sport Sci Rev 2011, 39:43-47.