Recombinant human parathyroid hormone (PTH 1-34) and low-intensity pulsed ultrasound have contrasting additive effects during fracture healing

Bone

Volumn 44, Issue 3, 2009, Pages 485-494

  Warden, Stuart J ^a,b   Komatsu, David E ^a,c   Rydberg, Johanna ^a   Bond, Julie L ^a   Hassett, Sean M ^a  

^a INDIANA UNIVERSITY   (United States)

^b INDIANA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c InMotion Musculoskeletal Institute   (United States)

Author keywords

Animal model; Orthopedics; Physical therapy; Teriparatide; Ultrasound therapy

Indexed keywords

PARATHYROID HORMONE[1-34]; PLACEBO; RECOMBINANT HORMONE; RECOMBINANT PARATHYROID HORMONE[1-34]; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ARTICLE; BONE MINERAL; CALLUS; CONTROLLED STUDY; FEMUR; FRACTURE HEALING; MALE; NONHUMAN; RAT; ULTRASOUND;

ANIMALS; COMBINED MODALITY THERAPY; FEMUR; FRACTURE HEALING; HUMANS; MALE; PEPTIDE FRAGMENTS; RANDOM ALLOCATION; RATS; RATS, SPRAGUE-DAWLEY; RECOMBINANT PROTEINS; STRESS, MECHANICAL; TERIPARATIDE; ULTRASONIC THERAPY;

EID: 59649083141     PISSN: 87563282     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bone.2008.11.007     Document Type: Article

References (60)

1. Lindsay R., Zhou H., Cosman F., Nieves J., Dempster D.W., and Hodsman A.B. Effects of a one-month treatment with PTH(1-34) on bone formation on cancellous, endocortical, and periosteal surfaces of the human ilium. J. Bone Miner. Res. 22 (2007) 495-502
2. Reeve J., Meunier P.J., Parsons J.A., Bernat M., Bijvoet O.L., Courpron P., et al. Anabolic effect of human parathyroid hormone fragment on trabecular bone in involutional osteoporosis: a multicentre trial. Br. Med. J. 280 (1980) 1340-1344
3. Neer R.M., Arnaud C.D., Zanchetta J.R., Prince R., Gaich G.A., Reginster J.Y., et al. Effect of parathyroid hormone (1-34) on fractures and bone mineral density in postmenopausal women with osteoporosis. N. Engl. J. Med. 344 (2001) 1434-1441
4. Barnes G.L., Kakar S., Vora S., Morgan E.F., Gerstenfeld L.C., and Einhorn T.A. Stimulation of fracture-healing with systemic intermittent parathyroid hormone treatment. J. Bone Joint. Surg. Am. 90 Suppl 1 (2008) 120-127
5. Chalidis B., Tzioupis C., Tsiridis E., and Giannoudis P.V. Enhancement of fracture healing with parathyroid hormone: preclinical studies and potential clinical applications. Expert Opin. Investig. Drugs. 16 (2007) 441-449
6. Skripitz R., and Aspenberg P. Parathyroid hormone-a drug for orthopedic surgery?. Acta Orthop. Scand. 75 (2004) 654-662
7. Alkhiary Y.M., Gerstenfeld L.C., Krall E., Westmore M., Sato M., Mitlak B.H., et al. Enhancement of experimental fracture-healing by systemic administration of recombinant human parathyroid hormone (PTH 1-34). J. Bone Joint. Surg. Am. 87 (2005) 731-741
8. Kakar S., Einhorn T.A., Vora S., Miara L.J., Hon G., Wigner N.A., et al. Enhanced chondrogenesis and Wnt-signaling in parathyroid hormone treated fractures. J. Bone Miner. Res. 22 (2007) 1903-1912
9. Nakajima A., Shimoji N., Shiomi K., Shimizu S., Moriya H., Einhorn T.A., et al. Mechanisms for the enhancement of fracture healing in rats treated with intermittent low-dose human parathyroid hormone (1-34). J. Bone Miner. Res. 17 (2002) 2038-2047
10. Warden S.J. A new direction for ultrasound therapy in sports medicine. Sports Med. 33 (2003) 95-107
11. Choi B.H., Choi M.H., Kwak M.G., Min B.H., Woo Z.H., et al. Mechanotransduction pathways of low-intensity ultrasound in C-28/I2 human chondrocyte cell line. Proc. Inst. Mech. Eng. [H] 221 (2007) 527-535
12. Naruse K., Mikuni-Takagaki Y., Azuma Y., Ito M., Ohta T., Kameyama K.Z., et al. Anabolic response of mouse bone-marrow-derived stromal cell clonal ST2 cells to low-intensity pulsed ultrasound. Biochem. Biophys. Res. Commun. 268 (2000) 216-220
13. Parvizi J., Wu C.C., Lewallen D.G., Greenleaf J.F., and Bolander M.E. Low-intensity ultrasound stimulates proteoglycan synthesis in rat chondrocytes by increasing aggrecan gene expression. J. Orthop. Res. 17 (1999) 488-494
14. Warden S.J., Favaloro J., Bennell K.L., McMeeken J.M., Ng K.W., Zajac J.D., and Wark J.D. Low-intensity pulsed ultrasound stimulates a bone-forming response in UMR-106 cells. Biochem. Biophys. Res. Commun. 286 (2001) 443-450
15. Heckman J.D., Ryaby J.P., McCabe J., Frey J.J., and Kilcoyne R.F. Acceleration of tibial fracture-healing by non-invasive, low-intensity pulsed ultrasound. J. Bone Joint. Surg. Am. 76A (1994) 26-34
16. Kristiansen T.K., Ryaby J.P., McCabe J., Frey J.J., and Roe L.R. Accelerated healing of distal radius fractures with the use of specific, low-intensity ultrasound. J. Bone Joint. Surg. Am. 79A (1997) 961-973
17. Mayr E., Rutzki M.M., Rutzki M., Borchardt B., Hausser H., and Rüter A. Beschleunigt niedrig intensiver, gepulster Ultraschall die Heilung von Skaphoidfrakturen?. Handchir. Mikrochir. Plast. Chir. 32 (2000) 115-122
18. Mayr E., Frankel V., and Rüter A. Ultrasound: an alternative healing method for nonunions?. Arch. Orthop. Trauma Surg. 120 (2000) 1-8
19. Nolte P.A., van der Krans A., Patka P., Janssen I.M.C., Ryaby J.P., and Albers G.H.R. Low-intensity pulsed ultrasound in the treatment of nonunions. J. Trauma 51 (2001) 693-702
20. Chow J.W.M., Fox S., Jagger C.J., and Chambers T.J. Role for parathyroid hormone in mechanical responsiveness of rat bone. Am. J. Physiol. 274 (1998) E146-E154
21. Hagino H., Okano T., Akhter M.P., Enokida M., and Teshima R. Effect of parathyroid hormone on cortical bone response to in vivo external loading of the rat tibia. J. Bone Miner. Metab. 19 (2001) 244-250
22. Kim C.H., Takai E., Zhou H., von Stechow D., Muller R., Dempster D.W., et al. Trabecular bone response to mechanical and parathyroid hormone stimulation: the role of mechanical microenvironment. J. Bone Miner. Res. 18 (2003) 2116-2125
23. Li J., Duncan R.L., Burr D.B., Gattone V.H., and Turner C.H. Parathyroid hormone enhances mechanically induced bone formation, possibly involving L-type voltage-sensitive calcium channels. Endocrinology 144 (2003) 1226-1233
24. Ma Y., Jee W.S., Yuan Z., Wei W., Chen H., Pun S., et al. Parathyroid hormone and mechanical usage have a synergistic effect in rat tibial diaphyseal cortical bone. J. Bone Miner. Res. 14 (1999) 439-448
25. Sugiyama T., Saxon L.K., Zaman G., Moustafa A., Sunters A., Price J.S., et al. Mechanical loading enhances the anabolic effects of intermittent parathyroid hormone (1-34) on trabecular and cortical bone in mice. Bone 43 (2008) 238-248
26. Gardner M.J., van der Meulen M.C., Carson J., Zelken J., Ricciardi B.F., Wright T.M., Lane J.M., and Bostrom M.P. Role of parathyroid hormone in the mechanosensitivity of fracture healing. J. Orthop. Res. 25 (2007) 1474-1480
27. Kaiser E., Sato M., Onyia J.E., and Chandrasekhar S. Parathyroid hormone (1-34) regulates integrin expression in vivo in rat osteoblasts. J. Cell. Biochem. 83 (2001) 617-630
28. Tang C.H., Yang R.S., Huang T.H., Lu D.Y., Chuang W.J., Huang T.F., et al. Ultrasound stimulates cyclooxygenase-2 expression and increases bone formation through integrin, focal adhesion kinase, phosphatidylinositol 3-kinase, and Akt pathway in osteoblasts. Mol. Pharmacol. 69 (2006) 2047-2057
29. Yamamoto T., Kambe F., Cao X., Lu X., Ishiguro N., and Seo H. Parathyroid hormone activates phosphoinositide 3-kinase-Akt-Bad cascade in osteoblast-like cells. Bone 40 (2007) 354-359
30. Bonnarens F., and Einhorn T.A. Production of a standard closed fracture in laboratory animal bone. J. Orthop. Res. 2 (1984) 97-101
31. Nakazawa T., Nakajima A., Shiomi K., Moriya H., Einhorn T.A., and Yamazaki M. Effects of low-dose, intermittent treatment with recombinant human parathyroid hormone (1-34) on chondrogenesis in a model of experimental fracture healing. Bone 37 (2005) 711-719
32. Frolik C.A., Black E.C., Cain R.L., Satterwhite J.H., Brown-Augsburger P.L., Sato M., et al. Anabolic and catabolic bone effects of human parathyroid hormone (1-34) are predicted by duration of hormone exposure. Bone 33 (2003) 372-379
33. Hu Z., Niu H., Yang X., Li H., Sang G., and Li B. Recombinant human parathyroid hormone 1-34: pharmacokinetics, tissue distribution and excretion in rats. Int. J. Pharm. 317 (2006) 144-154
34. Li J., Waugh L.J., Hui S.L., Burr D.B., and Warden S.J. Low-intensity pulsed ultrasound and nonsteroidal anti-inflammatory drugs have opposing effects during stress fracture repair. J. Orthop. Res. 25 (2007) 1559-1567
35. Warden S.J., Fuchs R.K., Kessler C.K., Avin K.G., Cardinal R.E., and Stewart R.L. Ultrasound produced by a conventional therapeutic ultrasound unit accelerates fracture repair. Phys. Ther. 86 (2006) 1118-1127
36. Turner C.H., and Burr D.B. Experimental techniques for bone mechanics. In: Cowin S.C. (Ed). Bone mechanics handbook. 2nd ed. (2001), CRC Press, Boca Raton, FL 7-1-7-35
37. Andreassen T.T., Ejersted C., and Oxlund H. Intermittent parathyroid hormone (1-34) treatment increases callus formation and mechanical strength of healing rat fractures. J. Bone Miner. Res. 14 (1999) 960-968
38. Andreassen T.T., Willick G.E., Morley P., and Whitfield J.F. Treatment with parathyroid hormone hPTH(1-34), hPTH(1-31), and monocyclic hPTH(1-31) enhances fracture strength and callus amount after withdrawal fracture strength and callus mechanical quality continue to increase. Calcif. Tissue Int. 74 (2004) 351-356
39. Holzer G., Majeska R.J., Lundy M.W., Hartke J.R., and Einhorn T.A. Parathyroid hormone enhances fracture healing. A preliminary report. Clin. Orthop. Relat. Res. 366 (1999) 258-263
40. Kaback L.A., Soung D.Y., Naik A., Geneau G., Schwarz E.M., Rosier R.N., et al. Teriparatide (1-34 human PTH) regulation of osterix during fracture repair. J. Cell. Biochem. 105 (2008) 219-226
41. Komatsubara S., Mori S., Mashiba T., Nonaka K., Seki A., Akiyama T., et al. Human parathyroid hormone (1-34) accelerates the fracture healing process of woven to lamellar bone replacement and new cortical shell formation in rat femora. Bone 36 (2005) 678-687
42. Manabe T., Mori S., Mashiba T., Kaji Y., Iwata K., Komatsubara S., et al. Human parathyroid hormone (1-34) accelerates natural fracture healing process in the femoral osteotomy model of cynomolgus monkeys. Bone 40 (2007) 1475-1482
43. Frolik C.A., Cain R.L., Sato M., Harvey A.K., Chandrasekhar S., Black E.C., et al. Comparison of recombinant human PTH(1-34) (LY333334) with a C-terminally substituted analog of human PTH-related protein(1-34) (RS-66271): in vitro activity and in vivo pharmacological effects in rats. J. Bone Miner. Res. 14 (1999) 163-172
44. Sato M., Zeng G.Q., Rowley E., and Turner C.H. LY353381 × HCl: an improved benzothiophene analog with bone efficacy complementary to parathyroid hormone-(1-34). Endocrinology 139 (1998) 4642-4651
45. Sato M., Zeng G.Q., and Turner C.H. Biosynthetic human parathyroid hormone (1-34) effects on bone quality in aged ovariectomized rats. Endocrinology 138 (1997) 4330-4337
46. Azuma Y., Ito M., Harada Y., Takagi H., Ohta T., and Jingushi S. Low-intensity pulsed ultrasound accelerates rat femoral fracture healing by acting on the various cellular reactions in the fracture callus. J. Bone Miner. Res. 16 (2001) 671-680
47. Pilla A.A., Mont M.A., Nasser P.R., Khan A., Figueiredo M., Kaufman J.J., et al. Non-invasive low-intensity pulsed ultrasound accelerates bone healing in the rabbit. J. Orthop. Trauma 4 (1990) 246-253
48. Takikawa S., Matsui N., Kokubu T., Tsunoda M., Fujioka H., Mizuno K., et al. Low-intensity pulsed ultrasound initiates bone healing in rat nonunion fracture model. J. Ultrasound Med. 20 (2001) 197-206
49. Wang S.-J., Lewallen D.G., Bolander M.E., Chao E.Y.S., Ilstrup D.M., and Greenleaf J.F. Low intensity ultrasound treatment increases strength in a rat femoral fracture model. J. Orthop. Res. 12 (1994) 40-47
50. Warden S.J., and McMeeken J.M. Ultrasound usage and dosage in sports physiotherapy. Ultrasound Med. Biol. 28 (2002) 1075-1080
51. Warden S.J., Bennell K.L., McMeeken J.M., and Wark J.D. Acceleration of fresh fracture repair using the sonic accelerated fracture healing system (SAFHS): a review. Calcif. Tissue Int. 66 (2000) 157-163
52. Busse J.W., and Bhandari M. Therapeutic ultrasound and fracture healing: a survey of beliefs and practices. Arch. Phys. Med. Rehabil. 85 (2004) 1653-1656
53. Gerstenfeld L.C., Wronski T.J., Hollinger J.O., and Einhorn T.A. Application of histomorphometric methods to the study of bone repair. J. Bone Miner. Res. 20 (2005) 1715-1722
54. Korstjens C.M., van der Rijt R.H., Albers G.H., Semeins C.M., and Klein-Nulend J. Low-intensity pulsed ultrasound affects human articular chondrocytes in vitro. Med Biol Eng Comput 46 (2008) 1263-1270
55. Takeuchi R., Ryo A., Komitsu N., Mikuni-Takagaki Y., Fukui A., Takagi Y., et al., Morishita S., Yamazaki Y., Kumagai K., Aoki I., Saito T. Low-intensity pulsed ultrasound activates the phosphatidylinositol 3 kinase/Akt pathway and stimulates the growth of chondrocytes in three-dimensional cultures: a basic science study. Arthritis Res. Ther. 10 (2008) R77
56. Wiltink A., Nijweide P.J., Oosterbaan W.A., Hekkenberg R.T., and Helders P.J.M. Effect of therapeutic ultrasound on endochondral ossification. Ultrasound Med. Biol. 21 (1995) 121-127
57. Chang W.H.S., Sun J.-S., Chang S.P., and Lin J.C. Study of the thermal effects of ultrasound stimulation on fracture healing. Bioelectromagnetics 23 (2002) 256-263
58. Zorlu Ü., Tercan M., Özyazgan I., Taskan I., Kardas Y., Balkar F., et al. Comparative study of the effect of ultrasound and electrostimulation on bone healing in rats. Am. J. Phys. Med. Rehabil. 77 (1998) 427-432
59. Dyson M., and Brookes M. Stimulation of bone repair by ultrasound. Ultrasound Med. Biol. Suppl. 2 (1983) 61-66
60. Yang K.H., Parvizi J., Wang S.-J., Lewallen D.G., Kinnick R.R., Greenleaf J.-F., and Bolander M.E. Exposure to low-intensity ultrasound increases aggrecan gene expression in a rat femur fracture model. J. Orthop. Res. 14 (1996) 802-809