Skip to main content
Erschienen in: Lasers in Medical Science 5/2012

01.09.2012 | Original Article

Effects of the combination of low-level laser irradiation and recombinant human bone morphogenetic protein-2 in bone repair

verfasst von: Anderson Paim Rosa, Luiz Gustavo de Sousa, Simone Cecilio Hallak Regalo, João Paulo Mardegan Issa, Ana Paula Amorim Barbosa, Dimitrius Leonardo Pitol, Richard Honorato de Oliveira, Paulo Batista de Vasconcelos, Fernando José Dias, Daniela Thomazatti Chimello, Selma Siéssere

Erschienen in: Lasers in Medical Science | Ausgabe 5/2012

Einloggen, um Zugang zu erhalten

Abstract

Low-level laser irradiation (LLLI) and recombinant human bone morphogenetic protein type 2 (rhBMP-2) have been used to stimulate bone formation. LLLI stimulates proliferation of osteoblast precursor cells and cell differentiation and rhBMP-2 recruits osteoprogenitor cells to the bone healing area. This in vivo study evaluated the effects of LLLI and rhBMP-2 on the bone healing process in rats. Critical bone defects were created in the parietal bone in 42 animals, and the animals were divided into six treatment groups: (1) laser, (2) 7 μg of rhBMP-2, (3) laser and 7 μg of rhBMP-2, (4) 7 μg of rhBMP-2/monoolein gel, (5) laser and 7 μg rhBMP-2/monoolein gel, and (6) critical bone defect controls. A gallium-aluminum-arsenide diode laser was used (wavelength 780 nm, output power 60 mW, beam area 0.04 cm2, irradiation time 80 s, energy density 120 J/cm2, irradiance 1.5 W/cm2). After 15 days, the calvarial tissues were removed for histomorphometric analysis. Group 3 defects showed higher amounts of newly formed bone (37.89%) than the defects of all the other groups (P < 0.05). The amounts of new bone in defects of groups 1 and 4 were not significantly different from each other (24.00% and 24.75%, respectively), but were significantly different from the amounts in the other groups (P < 0.05). The amounts of new bone in the defects of groups 2 and 5 were not significantly different from each other (31.42% and 31.96%, respectively), but were significantly different from the amounts in the other groups (P < 0.05). Group 6 defects had 14.10% new bone formation, and this was significantly different from the amounts in the other groups (P < 0.05). It can be concluded that LLLI administered during surgery effectively accelerated healing of critical bone defects filled with pure rhBMP-2, achieving a better result than LLLI alone or the use of rhBMP-2 alone.
Literatur
1.
Zurück zum Zitat Stein A, Benayahu D, Maltz L, Oron U (2005) Low-level laser irradiation promotes proliferation and differentiation of human osteoblasts in vitro. Photomed Laser Surg 23:161–166PubMedCrossRef Stein A, Benayahu D, Maltz L, Oron U (2005) Low-level laser irradiation promotes proliferation and differentiation of human osteoblasts in vitro. Photomed Laser Surg 23:161–166PubMedCrossRef
2.
Zurück zum Zitat Ozawa Y, Shimizu N, Kariya G, Abiko Y (1998) Low-energy laser irradiation stimulates bone nodule formation at early stages of cell culture in rat calvarial cells. Bone 22:347–354PubMedCrossRef Ozawa Y, Shimizu N, Kariya G, Abiko Y (1998) Low-energy laser irradiation stimulates bone nodule formation at early stages of cell culture in rat calvarial cells. Bone 22:347–354PubMedCrossRef
3.
Zurück zum Zitat Shegarfi H, Reikeras O (2009) Review article: bone transplantation and immune response. J Orthop Surg 17:206–211 Shegarfi H, Reikeras O (2009) Review article: bone transplantation and immune response. J Orthop Surg 17:206–211
4.
Zurück zum Zitat Toriumi DM, Robertson K (1993) Bone inductive biomaterials in facial plastic and reconstructive surgery. Facial Plast Surg 9:29–36PubMedCrossRef Toriumi DM, Robertson K (1993) Bone inductive biomaterials in facial plastic and reconstructive surgery. Facial Plast Surg 9:29–36PubMedCrossRef
5.
Zurück zum Zitat Bostrom MP, Saleh KJ, Einhorn TA (1999) Osteoinductive growth factors in preclinical fracture and long bone defects models. Orthop Clin N Am 30:647–658CrossRef Bostrom MP, Saleh KJ, Einhorn TA (1999) Osteoinductive growth factors in preclinical fracture and long bone defects models. Orthop Clin N Am 30:647–658CrossRef
6.
Zurück zum Zitat Canto FRT, Garcia SB, Issa JPM, Marin A, Guimarães EABB, Defino HLA (2008) Influence of decortication of the recipient graft bed on graft integration and tissue neoformation in the graft-recipient bed interface. Eur Spine J 17:706–714PubMedCrossRef Canto FRT, Garcia SB, Issa JPM, Marin A, Guimarães EABB, Defino HLA (2008) Influence of decortication of the recipient graft bed on graft integration and tissue neoformation in the graft-recipient bed interface. Eur Spine J 17:706–714PubMedCrossRef
7.
Zurück zum Zitat Arosarena O, Collins W (2005) Comparison of BMP-2 and -4 for rat mandibular bone regeneration at various doses. Orthod Craniofac Res 8:267–276PubMedCrossRef Arosarena O, Collins W (2005) Comparison of BMP-2 and -4 for rat mandibular bone regeneration at various doses. Orthod Craniofac Res 8:267–276PubMedCrossRef
8.
Zurück zum Zitat Issa JPM, Nascimento C, Bentley MV, Guimarães EABB, Iyomasa MM, Sebald W, Albuquerque RF Jr (2007) Bone repair in rat mandible by rhBMP-2 associated with two carriers. Micron 39:373–379PubMedCrossRef Issa JPM, Nascimento C, Bentley MV, Guimarães EABB, Iyomasa MM, Sebald W, Albuquerque RF Jr (2007) Bone repair in rat mandible by rhBMP-2 associated with two carriers. Micron 39:373–379PubMedCrossRef
9.
Zurück zum Zitat Issa JP, Defino HL, Netto JC, Volpon JB, Regalo SC, Iyomasa MM, Siéssere S, Tiossi R (2010) Evaluation of rhBMP-2 and natural latex as potential osteogenic proteins in critical size defects by histomorphometric methods. Anat Rec 293:794–801CrossRef Issa JP, Defino HL, Netto JC, Volpon JB, Regalo SC, Iyomasa MM, Siéssere S, Tiossi R (2010) Evaluation of rhBMP-2 and natural latex as potential osteogenic proteins in critical size defects by histomorphometric methods. Anat Rec 293:794–801CrossRef
10.
Zurück zum Zitat Albuquerque RF Jr, Oliveira MTM, Guimarães EABB, Brentegani LG, Issa JPM (2008) Trigeminal nitric oxide synthase expression correlates with new bone formation during distraction osteogenesis. Calcif Tissue Int 82:309–315PubMedCrossRef Albuquerque RF Jr, Oliveira MTM, Guimarães EABB, Brentegani LG, Issa JPM (2008) Trigeminal nitric oxide synthase expression correlates with new bone formation during distraction osteogenesis. Calcif Tissue Int 82:309–315PubMedCrossRef
11.
Zurück zum Zitat Issa JPM, Nascimento C, Lamano-Carvalho TL, Iyomasa MM, Sebald W, Albuquerque RF Jr (2009) Effect of recombinant human bone morphogenetic protein-2 on bone formation in the acute distraction osteogenesis. Clin Oral Implant Res 20:1286–1292CrossRef Issa JPM, Nascimento C, Lamano-Carvalho TL, Iyomasa MM, Sebald W, Albuquerque RF Jr (2009) Effect of recombinant human bone morphogenetic protein-2 on bone formation in the acute distraction osteogenesis. Clin Oral Implant Res 20:1286–1292CrossRef
12.
Zurück zum Zitat Hally A (1964) A counting method for measuring the volumes of tissue components in microscopical sections. Q J Microsc Sci 105:503–517 Hally A (1964) A counting method for measuring the volumes of tissue components in microscopical sections. Q J Microsc Sci 105:503–517
13.
Zurück zum Zitat Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30:23–38PubMedCrossRef Weibel ER, Kistler GS, Scherle WF (1966) Practical stereological methods for morphometric cytology. J Cell Biol 30:23–38PubMedCrossRef
14.
Zurück zum Zitat Mandarim-de-Lacerda CA (1995) Métodos quantitativos em morfologia. Eduerj, Rio de Janeiro Mandarim-de-Lacerda CA (1995) Métodos quantitativos em morfologia. Eduerj, Rio de Janeiro
15.
Zurück zum Zitat Carvalho PTC, Silva IS, Reis FA, Belchior ACG, Facco GG, Guimarães RN, Fernandes GHC, Denadai AS (2006) Effect of 650 nm low-power laser on bone morphogenetic protein in bone defects induced in rat femors. Acta Cir Bras 21:63–68CrossRef Carvalho PTC, Silva IS, Reis FA, Belchior ACG, Facco GG, Guimarães RN, Fernandes GHC, Denadai AS (2006) Effect of 650 nm low-power laser on bone morphogenetic protein in bone defects induced in rat femors. Acta Cir Bras 21:63–68CrossRef
16.
Zurück zum Zitat Siéssere S, Sousa LG, Issa JP, Iyomasa MM, Pitol DL, Barbosa AP, Semprini M, Sebald W, Bentley MV, Regalo SC (2011) Application of low-level laser irradiation (LLLI) and rhBMP-2 in critical bone defect of ovariectomized rats: histomorphometric evaluation. Photomed Laser Surg 29:453–458. doi:10.1089/pho.2010.2917 PubMedCrossRef Siéssere S, Sousa LG, Issa JP, Iyomasa MM, Pitol DL, Barbosa AP, Semprini M, Sebald W, Bentley MV, Regalo SC (2011) Application of low-level laser irradiation (LLLI) and rhBMP-2 in critical bone defect of ovariectomized rats: histomorphometric evaluation. Photomed Laser Surg 29:453–458. doi:10.​1089/​pho.​2010.​2917 PubMedCrossRef
17.
Zurück zum Zitat Guzzardella GA, Fini M, Torricelli P, Giavaresi G, Giardino R (2002) Laser stimulation on bone defect healing: an in vitro study. Lasers Med Sci 17:216–220PubMedCrossRef Guzzardella GA, Fini M, Torricelli P, Giavaresi G, Giardino R (2002) Laser stimulation on bone defect healing: an in vitro study. Lasers Med Sci 17:216–220PubMedCrossRef
18.
Zurück zum Zitat Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultrastructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40:413–418PubMedCrossRef Iyomasa DM, Garavelo I, Iyomasa MM, Watanabe IS, Issa JP (2009) Ultrastructural analysis of the low level laser therapy effects on the lesioned anterior tibial muscle in the gerbil. Micron 40:413–418PubMedCrossRef
19.
Zurück zum Zitat Spector JA, Luchs JS, Mehrara BJ, Greenwald JA, Smith LP, Longaker MT (2001) Expression of bone morphogenetic proteins during membranous bone healing. Plast Reconstr Surg 107:124–134PubMedCrossRef Spector JA, Luchs JS, Mehrara BJ, Greenwald JA, Smith LP, Longaker MT (2001) Expression of bone morphogenetic proteins during membranous bone healing. Plast Reconstr Surg 107:124–134PubMedCrossRef
20.
Zurück zum Zitat Ruhe PQ, Kroese-Deutman HC, Wolke JG, Spauwen PH, Jansen JA (2004) Bone inductive properties of rhBMP-2 loaded porous calcium phosphate cement implants in cranial defects in rabbits. Biomaterials 25:2123–2132PubMedCrossRef Ruhe PQ, Kroese-Deutman HC, Wolke JG, Spauwen PH, Jansen JA (2004) Bone inductive properties of rhBMP-2 loaded porous calcium phosphate cement implants in cranial defects in rabbits. Biomaterials 25:2123–2132PubMedCrossRef
21.
Zurück zum Zitat Gerbi ME, Marques AM, Ramalho LM, Ponzi EA, Carvalho CM, Santos RC, Oliveira PC, Nóia M, Pinheiro AL (2008) Infrared laser light further improves bone healing when associated with bone morphogenic proteins: an in vivo study in a rodent model. Photomed Laser Surg 26:55–60PubMedCrossRef Gerbi ME, Marques AM, Ramalho LM, Ponzi EA, Carvalho CM, Santos RC, Oliveira PC, Nóia M, Pinheiro AL (2008) Infrared laser light further improves bone healing when associated with bone morphogenic proteins: an in vivo study in a rodent model. Photomed Laser Surg 26:55–60PubMedCrossRef
22.
Zurück zum Zitat Denadai AS, Carvalho PTC, Reis FA, Belchior ACG, Pereira DM, Dourado DM, Silva IS, Oliveira LVF (2009) Morphometric and histological analysis of low-power laser influence on bone morphogenetic protein in bone defects repair. Laser Med Sci 24:689–695. doi:10.1007/s10103-008-0595-6 CrossRef Denadai AS, Carvalho PTC, Reis FA, Belchior ACG, Pereira DM, Dourado DM, Silva IS, Oliveira LVF (2009) Morphometric and histological analysis of low-power laser influence on bone morphogenetic protein in bone defects repair. Laser Med Sci 24:689–695. doi:10.​1007/​s10103-008-0595-6 CrossRef
23.
Zurück zum Zitat Saracino S, Mozzati M, Martinasso G, Pol R, Canuto RA, Muzio G (2009) Superpulsed laser irradiation increases osteoblast activity via modulation of bone morphogenetic factors. Lasers Surg Med 41:298–304PubMedCrossRef Saracino S, Mozzati M, Martinasso G, Pol R, Canuto RA, Muzio G (2009) Superpulsed laser irradiation increases osteoblast activity via modulation of bone morphogenetic factors. Lasers Surg Med 41:298–304PubMedCrossRef
24.
Zurück zum Zitat Pretel H, Lizarelli RF, Ramalho LT (2007) Effect of low-level laser therapy on bone repair: histological study in rats. Lasers Surg Med 39:788–796PubMedCrossRef Pretel H, Lizarelli RF, Ramalho LT (2007) Effect of low-level laser therapy on bone repair: histological study in rats. Lasers Surg Med 39:788–796PubMedCrossRef
25.
Zurück zum Zitat Garavello-Freitas I, Baranauskas V, Joazeiro PP, Padovani CR, Dal Pai-Silva M, da Cruz-Hofling MA (2003) Low-power laser irradiation improves histomorphometrical parameters and bone matrix organization during tibia wound healing in rats. J Photochem Photobiol B 70:81–89PubMedCrossRef Garavello-Freitas I, Baranauskas V, Joazeiro PP, Padovani CR, Dal Pai-Silva M, da Cruz-Hofling MA (2003) Low-power laser irradiation improves histomorphometrical parameters and bone matrix organization during tibia wound healing in rats. J Photochem Photobiol B 70:81–89PubMedCrossRef
26.
Zurück zum Zitat Pinheiro AL, Limeira Junior Fde A, Gerbi ME, Ramalho LM, Marzola C, Ponzi EA, Soares AO, De Carvalho LC, Lima HC, Gonçalves TO (2003) Effect of 830-nm laser light on the repair of bone defects grafted with inorganic bovine bone and decalcified cortical osseous membrane. J Clin Laser Med Surg 21:301–306PubMedCrossRef Pinheiro AL, Limeira Junior Fde A, Gerbi ME, Ramalho LM, Marzola C, Ponzi EA, Soares AO, De Carvalho LC, Lima HC, Gonçalves TO (2003) Effect of 830-nm laser light on the repair of bone defects grafted with inorganic bovine bone and decalcified cortical osseous membrane. J Clin Laser Med Surg 21:301–306PubMedCrossRef
27.
Zurück zum Zitat Karu T, Pyatibrat L, Kalendo G (1995) Irradiation with He-Ne laser increases ATP level in cells cultivated in vitro. J Photochem Photobiol B 27:219–223PubMedCrossRef Karu T, Pyatibrat L, Kalendo G (1995) Irradiation with He-Ne laser increases ATP level in cells cultivated in vitro. J Photochem Photobiol B 27:219–223PubMedCrossRef
28.
Zurück zum Zitat Khadra M, Kasem N, Haanaes HR, Ellingsen JE, Lyngstadaas SP (2004) Enhancement of bone formation in rat calvarial bone defects using low-level laser therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97:693–700PubMedCrossRef Khadra M, Kasem N, Haanaes HR, Ellingsen JE, Lyngstadaas SP (2004) Enhancement of bone formation in rat calvarial bone defects using low-level laser therapy. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 97:693–700PubMedCrossRef
29.
Zurück zum Zitat Renno AC, de Moura FM, dos Santos NS, Tirico RP, Bossini PS, Parizotto NA (2006) Effects of 830-nm laser light on preventing bone loss after ovariectomy. Photomed Laser Surg 24:642–645PubMedCrossRef Renno AC, de Moura FM, dos Santos NS, Tirico RP, Bossini PS, Parizotto NA (2006) Effects of 830-nm laser light on preventing bone loss after ovariectomy. Photomed Laser Surg 24:642–645PubMedCrossRef
30.
Zurück zum Zitat Riley EH, Lane JM, Urist MR, Lyons KM, Lieberman JR (1996) Bone morphogenetic protein-2: biology and applications. Clin Orthop Relat Res 324:39–46PubMedCrossRef Riley EH, Lane JM, Urist MR, Lyons KM, Lieberman JR (1996) Bone morphogenetic protein-2: biology and applications. Clin Orthop Relat Res 324:39–46PubMedCrossRef
31.
Zurück zum Zitat Okubo Y, Bessho K, Fujimura K, Kusumoto K, Ogawa Y, Iizuka T (2000) Osteogenesis by recombinant human bone morphogenetic protein-2 at skeletal sites. Clin Orthop Relat Res 375:295–301PubMedCrossRef Okubo Y, Bessho K, Fujimura K, Kusumoto K, Ogawa Y, Iizuka T (2000) Osteogenesis by recombinant human bone morphogenetic protein-2 at skeletal sites. Clin Orthop Relat Res 375:295–301PubMedCrossRef
32.
Zurück zum Zitat Murakami N, Saito N, Horiuchi H, Okada T, Nozaki K, Takaoka K (2002) Repair of segmental defects in rabbit humeri with titanium fiber mesh cylinders containing recombinant human bone morphogenetic protein-2 (rhBMP-2) and a synthetic polymer. J Biomed Mater Res 62:169–174PubMedCrossRef Murakami N, Saito N, Horiuchi H, Okada T, Nozaki K, Takaoka K (2002) Repair of segmental defects in rabbit humeri with titanium fiber mesh cylinders containing recombinant human bone morphogenetic protein-2 (rhBMP-2) and a synthetic polymer. J Biomed Mater Res 62:169–174PubMedCrossRef
33.
Zurück zum Zitat Issa JP, Pitol DL, Iyomasa MM, Barbosa AP, Defino HL, Volpon JB, Shimano AC, Silva P (2009) Collagen fibers evaluation after rhBMP-2 insertion in critical-sized defects. Micron 40:560–562PubMedCrossRef Issa JP, Pitol DL, Iyomasa MM, Barbosa AP, Defino HL, Volpon JB, Shimano AC, Silva P (2009) Collagen fibers evaluation after rhBMP-2 insertion in critical-sized defects. Micron 40:560–562PubMedCrossRef
34.
Zurück zum Zitat Wang EA, Rosen V, D’Alessandro JS, Bauduy M, Cordes P, Harada T, Israel D, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, Mcquaid D, Moutsatsos IK, Nove J, Wozney JM (1990) Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220–2224PubMedCrossRef Wang EA, Rosen V, D’Alessandro JS, Bauduy M, Cordes P, Harada T, Israel D, Hewick RM, Kerns KM, LaPan P, Luxenberg DP, Mcquaid D, Moutsatsos IK, Nove J, Wozney JM (1990) Recombinant human bone morphogenetic protein induces bone formation. Proc Natl Acad Sci USA 87:2220–2224PubMedCrossRef
35.
Zurück zum Zitat Abdala PM, Iyomasa MM, Sato S, Bentley MV, Pitol DL, Regalo SC, Siéssere S, Issa JP (2010) Osteoinductivity potential of rhBMP-2 associated with two carriers in different dosages. Anat Sci Int 85:181–188PubMedCrossRef Abdala PM, Iyomasa MM, Sato S, Bentley MV, Pitol DL, Regalo SC, Siéssere S, Issa JP (2010) Osteoinductivity potential of rhBMP-2 associated with two carriers in different dosages. Anat Sci Int 85:181–188PubMedCrossRef
36.
Zurück zum Zitat D’Antona P, Parker WO, Zanirato MC, Esposito E, Nastruzzi C (2000) Rheologic and NMR characterization of monoglyceride-based formulations. J Biomed Mater Res 52:40–52PubMedCrossRef D’Antona P, Parker WO, Zanirato MC, Esposito E, Nastruzzi C (2000) Rheologic and NMR characterization of monoglyceride-based formulations. J Biomed Mater Res 52:40–52PubMedCrossRef
37.
Zurück zum Zitat Boyd BJ, Whittaker DV, Khoo SM, Davey G (2006) Lyotropic liquid crystalline phases formed from glycerate surfactants as sustained release drug delivery systems. Int J Pharm 309:218–226PubMedCrossRef Boyd BJ, Whittaker DV, Khoo SM, Davey G (2006) Lyotropic liquid crystalline phases formed from glycerate surfactants as sustained release drug delivery systems. Int J Pharm 309:218–226PubMedCrossRef
Metadaten
Titel
Effects of the combination of low-level laser irradiation and recombinant human bone morphogenetic protein-2 in bone repair
verfasst von
Anderson Paim Rosa
Luiz Gustavo de Sousa
Simone Cecilio Hallak Regalo
João Paulo Mardegan Issa
Ana Paula Amorim Barbosa
Dimitrius Leonardo Pitol
Richard Honorato de Oliveira
Paulo Batista de Vasconcelos
Fernando José Dias
Daniela Thomazatti Chimello
Selma Siéssere
Publikationsdatum
01.09.2012
Verlag
Springer-Verlag
Erschienen in
Lasers in Medical Science / Ausgabe 5/2012
Print ISSN: 0268-8921
Elektronische ISSN: 1435-604X
DOI
https://doi.org/10.1007/s10103-011-1022-y

Weitere Artikel der Ausgabe 5/2012

Lasers in Medical Science 5/2012 Zur Ausgabe