Skip to main content
Erschienen in: Clinical Oral Investigations 4/2019

30.08.2018 | Original Article

Evaluation of bone turnover after bisphosphonate withdrawal and its influence on implant osseointegration: an in vivo study in rats

verfasst von: Fausto Frizzera, Mario Henrique Arruda Verzola, Rafael Scaf de Molon, Guilherme Jose Pimentel Lopes de Oliveira, Gabriela Giro, Luis Carlos Spolidorio, Rosa Maria Rodrigues Pereira, Sotirios Tetradis, Joni Augusto Cirelli, Silvana Regina Peres Orrico

Erschienen in: Clinical Oral Investigations | Ausgabe 4/2019

Einloggen, um Zugang zu erhalten

Abstract

Objectives

The aim of this study was to investigate bone turnover alterations after alendronate (ALD) withdrawal and its influence on dental implants osseointegration.

Materials and methods

Seventy female Wistar rats were randomly divided in 2 groups that received on day 0 either placebo (control group—CTL; n = 10) or 1 mg/kg sodium alendronate (ALD; n = 60) once a week for 4 months. At day 120, ALD treatment was suspended for 50 animals. Then, a titanium implant was placed in the left tibia of each rat that were randomly allocated in five subgroups of ten animals each, according to the period of evaluation: day 0 (INT-0), day 7 (INT-7), day 14 (INT-14), day 28 (INT-28), and day 45 (INT-45) after ALD withdrawal. CTL group and a group that received ALD until the end of the experimental period (non-interrupted group—non-INT; n = 10) underwent implant placement on day 120. Animals were euthanized 28 days after implant surgery. Bone mineral density (BMD) of femur and lumbar vertebrae were evaluated by DXA, biochemical markers of bone turnover were analyzed by ELISA, and bone histomorphometry was performed to measure bone-to-implant contact (BIC) and bone area fraction occupancy (BAFO).

Results

All groups receiving ALD showed higher BMD values when compared to CTL group, which were maintained after its withdrawal. Decreased concentrations in all bone turnover markers were observed in the non-INT group, and in the groups in which ALD was discontinued compared to the CTL group. The non-INT group showed lower %BIC and notably changes in bone quality, which was persistent after drug withdrawal.

Conclusion

Collectively, the findings of this study demonstrated that ALD therapy decreased bone turnover and impaired bone quality and quantity around dental implants, and that its discontinuation did not reverse these findings.

Clinical relevance

The severe suppression of bone turnover caused by the prolonged use of ALD may alter the capacity of bone tissue to integrate with the implant threads impairing the osseointegration process.
Anhänge
Nur mit Berechtigung zugänglich
Literatur
1.
Zurück zum Zitat Luckman SP, Hughes DE, Coxon FP, Graham R, Russell G, Rogers MJ (1998) Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 13:581–589CrossRefPubMed Luckman SP, Hughes DE, Coxon FP, Graham R, Russell G, Rogers MJ (1998) Nitrogen-containing bisphosphonates inhibit the mevalonate pathway and prevent post-translational prenylation of GTP-binding proteins, including Ras. J Bone Miner Res 13:581–589CrossRefPubMed
2.
Zurück zum Zitat Kimmel DB (2007) Mechanism of action, pharmacokinetic and pharmacodynamic profile, and clinical applications of nitrogen-containing bisphosphonates. J Dent Res 86:1022–1033CrossRefPubMed Kimmel DB (2007) Mechanism of action, pharmacokinetic and pharmacodynamic profile, and clinical applications of nitrogen-containing bisphosphonates. J Dent Res 86:1022–1033CrossRefPubMed
3.
Zurück zum Zitat Soundia A, Hadaya D, Esfandi N, de Molon RS, Bezouglaia O, Dry SM, Pirih FQ, Aghaloo T, Tetradis S (2016) Osteonecrosis of the jaws (ONJ) in mice after extraction of teeth with periradicular disease. Bone 90:133–141CrossRefPubMedPubMedCentral Soundia A, Hadaya D, Esfandi N, de Molon RS, Bezouglaia O, Dry SM, Pirih FQ, Aghaloo T, Tetradis S (2016) Osteonecrosis of the jaws (ONJ) in mice after extraction of teeth with periradicular disease. Bone 90:133–141CrossRefPubMedPubMedCentral
4.
Zurück zum Zitat Tella SH, Gallagher JC (2014) Prevention and treatment of postmenopausal osteoporosis. J Steroid Biochem Mol Biol 142:155–170CrossRefPubMed Tella SH, Gallagher JC (2014) Prevention and treatment of postmenopausal osteoporosis. J Steroid Biochem Mol Biol 142:155–170CrossRefPubMed
5.
Zurück zum Zitat Tolia M, Zygogianni A, Kouvaris JR, Meristoudis C, Margari N, Karakitsos P, Kokakis I, Kardamakis D, Papadimitriou C, Mystakidou K, Tsoukalas N, Kyrgias G, Armonis B, Filippiadis DK, Kelekis AD, Kelekis N, Kouloulias V (2014) The key role of bisphosphonates in the supportive care of cancer patients. Anticancer Res 34:23–37PubMed Tolia M, Zygogianni A, Kouvaris JR, Meristoudis C, Margari N, Karakitsos P, Kokakis I, Kardamakis D, Papadimitriou C, Mystakidou K, Tsoukalas N, Kyrgias G, Armonis B, Filippiadis DK, Kelekis AD, Kelekis N, Kouloulias V (2014) The key role of bisphosphonates in the supportive care of cancer patients. Anticancer Res 34:23–37PubMed
6.
Zurück zum Zitat Russell G, Mueller G, Shipman C, Croucher P (2001) Clinical disorders of bone resorption. Novartis Found Symp 232:251–267 discussion 267-271PubMed Russell G, Mueller G, Shipman C, Croucher P (2001) Clinical disorders of bone resorption. Novartis Found Symp 232:251–267 discussion 267-271PubMed
7.
Zurück zum Zitat Wang HL, Weber D, McCauley LK (2007) Effect of long-term oral bisphosphonates on implant wound healing: literature review and a case report. J Periodontol 78:584–594CrossRefPubMed Wang HL, Weber D, McCauley LK (2007) Effect of long-term oral bisphosphonates on implant wound healing: literature review and a case report. J Periodontol 78:584–594CrossRefPubMed
9.
Zurück zum Zitat Vohra F, Al-Rifaiy MQ, Almas K, Javed F (2014) Efficacy of systemic bisphosphonate delivery on osseointegration of implants under osteoporotic conditions: lessons from animal studies. Arch Oral Biol 59:912–920CrossRefPubMed Vohra F, Al-Rifaiy MQ, Almas K, Javed F (2014) Efficacy of systemic bisphosphonate delivery on osseointegration of implants under osteoporotic conditions: lessons from animal studies. Arch Oral Biol 59:912–920CrossRefPubMed
10.
Zurück zum Zitat Adler RA, El-Hajj Fuleihan G, Bauer DC, Camacho PM, Clarke BL, Clines GA, Compston JE, Drake MT, Edwards BJ, Favus MJ, Greenspan SL, McKinney R Jr, Pignolo RJ, Sellmeyer DE (2016) Managing osteoporosis in patients on long-term bisphosphonate treatment: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 31:16–35CrossRefPubMed Adler RA, El-Hajj Fuleihan G, Bauer DC, Camacho PM, Clarke BL, Clines GA, Compston JE, Drake MT, Edwards BJ, Favus MJ, Greenspan SL, McKinney R Jr, Pignolo RJ, Sellmeyer DE (2016) Managing osteoporosis in patients on long-term bisphosphonate treatment: report of a task force of the American Society for Bone and Mineral Research. J Bone Miner Res 31:16–35CrossRefPubMed
11.
Zurück zum Zitat Shirota T, Tashiro M, Ohno K, Yamaguchi A (2003) Effect of intermittent parathyroid hormone (1-34) treatment on the bone response after placement of titanium implants into the tibia of ovariectomized rats. J Oral Maxillofac Surg 61:471–480CrossRefPubMed Shirota T, Tashiro M, Ohno K, Yamaguchi A (2003) Effect of intermittent parathyroid hormone (1-34) treatment on the bone response after placement of titanium implants into the tibia of ovariectomized rats. J Oral Maxillofac Surg 61:471–480CrossRefPubMed
12.
Zurück zum Zitat Tokugawa Y, Shirota T, Ohno K, Yamaguchi A (2003) Effects of bisphosphonate on bone reaction after placement of titanium implants in tibiae of ovariectomized rats. Int J Oral Maxillofac Implants 18:66–74PubMed Tokugawa Y, Shirota T, Ohno K, Yamaguchi A (2003) Effects of bisphosphonate on bone reaction after placement of titanium implants in tibiae of ovariectomized rats. Int J Oral Maxillofac Implants 18:66–74PubMed
13.
Zurück zum Zitat Yamazaki M, Shirota T, Tokugawa Y, Motohashi M, Ohno K, Michi K, Yamaguchi A (1999) Bone reactions to titanium screw implants in ovariectomized animals. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 87:411–418CrossRefPubMed Yamazaki M, Shirota T, Tokugawa Y, Motohashi M, Ohno K, Michi K, Yamaguchi A (1999) Bone reactions to titanium screw implants in ovariectomized animals. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 87:411–418CrossRefPubMed
14.
Zurück zum Zitat Pan J, Shirota T, Ohno K, Michi K (2000) Effect of ovariectomy on bone remodeling adjacent to hydroxyapatite-coated implants in the tibia of mature rats. J Oral Maxillofac Surg 58:877–882CrossRefPubMed Pan J, Shirota T, Ohno K, Michi K (2000) Effect of ovariectomy on bone remodeling adjacent to hydroxyapatite-coated implants in the tibia of mature rats. J Oral Maxillofac Surg 58:877–882CrossRefPubMed
15.
Zurück zum Zitat Carvalho MD, Benatti BB, Cesar-Neto JB, Nociti FH, Jr., da Rocha Nogueira Filho G, Casati MZ, Sallum EA (2006) Effect of cigarette smoke inhalation and estrogen deficiency on bone healing around titanium implants: a histometric study in rats. J Periodontol 77:599–605 Carvalho MD, Benatti BB, Cesar-Neto JB, Nociti FH, Jr., da Rocha Nogueira Filho G, Casati MZ, Sallum EA (2006) Effect of cigarette smoke inhalation and estrogen deficiency on bone healing around titanium implants: a histometric study in rats. J Periodontol 77:599–605
16.
Zurück zum Zitat Duarte PM, Cesar Neto JB, Goncalves PF, Sallum EA, Nociti j F (2003) Estrogen deficiency affects bone healing around titanium implants: a histometric study in rats. Implant Dent 12:340–346CrossRefPubMed Duarte PM, Cesar Neto JB, Goncalves PF, Sallum EA, Nociti j F (2003) Estrogen deficiency affects bone healing around titanium implants: a histometric study in rats. Implant Dent 12:340–346CrossRefPubMed
17.
Zurück zum Zitat Nociti FH Jr, Sallum AW, Sallum EA, Duarte PM (2002) Effect of estrogen replacement and calcitonin therapies on bone around titanium implants placed in ovariectomized rats: a histometric study. Int J Oral Maxillofac Implants 17:786–792PubMed Nociti FH Jr, Sallum AW, Sallum EA, Duarte PM (2002) Effect of estrogen replacement and calcitonin therapies on bone around titanium implants placed in ovariectomized rats: a histometric study. Int J Oral Maxillofac Implants 17:786–792PubMed
18.
Zurück zum Zitat Giro G, Coelho PG, Pereira RM, Jorgetti V, Marcantonio E Jr, Orrico SR (2011) The effect of oestrogen and alendronate therapies on postmenopausal bone loss around osseointegrated titanium implants. Clin Oral Implants Res 22:259–264CrossRefPubMed Giro G, Coelho PG, Pereira RM, Jorgetti V, Marcantonio E Jr, Orrico SR (2011) The effect of oestrogen and alendronate therapies on postmenopausal bone loss around osseointegrated titanium implants. Clin Oral Implants Res 22:259–264CrossRefPubMed
19.
Zurück zum Zitat Giro G, Goncalves D, Sakakura CE, Pereira RM, Marcantonio Junior E, Orrico SR (2008) Influence of estrogen deficiency and its treatment with alendronate and estrogen on bone density around osseointegrated implants: radiographic study in female rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105:162–167CrossRefPubMed Giro G, Goncalves D, Sakakura CE, Pereira RM, Marcantonio Junior E, Orrico SR (2008) Influence of estrogen deficiency and its treatment with alendronate and estrogen on bone density around osseointegrated implants: radiographic study in female rats. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 105:162–167CrossRefPubMed
20.
Zurück zum Zitat Verzola MH, Frizzera F, de Oliveira GJ, Pereira RM, Rodrigues-Filho UP, Nonaka KO, Orrico SR (2015) Effects of the long-term administration of alendronate on the mechanical properties of the basal bone and on osseointegration. Clin Oral Implants Res 26:1466–1475CrossRefPubMed Verzola MH, Frizzera F, de Oliveira GJ, Pereira RM, Rodrigues-Filho UP, Nonaka KO, Orrico SR (2015) Effects of the long-term administration of alendronate on the mechanical properties of the basal bone and on osseointegration. Clin Oral Implants Res 26:1466–1475CrossRefPubMed
21.
Zurück zum Zitat Viera-Negron YE, Ruan WH, Winger JN, Hou X, Sharawy MM, Borke JL (2008) Effect of ovariectomy and alendronate on implant osseointegration in rat maxillary bone. J Oral Implantol 34:76–82CrossRefPubMed Viera-Negron YE, Ruan WH, Winger JN, Hou X, Sharawy MM, Borke JL (2008) Effect of ovariectomy and alendronate on implant osseointegration in rat maxillary bone. J Oral Implantol 34:76–82CrossRefPubMed
22.
Zurück zum Zitat Giro G, Sakakura CE, Goncalves D, Pereira RM, Marcantonio E Jr, Orrico SR (2007) Effect of 17beta-estradiol and alendronate on the removal torque of osseointegrated titanium implants in ovariectomized rats. J Periodontol 78:1316–1321CrossRefPubMed Giro G, Sakakura CE, Goncalves D, Pereira RM, Marcantonio E Jr, Orrico SR (2007) Effect of 17beta-estradiol and alendronate on the removal torque of osseointegrated titanium implants in ovariectomized rats. J Periodontol 78:1316–1321CrossRefPubMed
23.
Zurück zum Zitat Chacon GE, Stine EA, Larsen PE, Beck FM, McGlumphy EA (2006) Effect of alendronate on endosseous implant integration: an in vivo study in rabbits. J Oral Maxillofac Surg 64:1005–1009CrossRefPubMed Chacon GE, Stine EA, Larsen PE, Beck FM, McGlumphy EA (2006) Effect of alendronate on endosseous implant integration: an in vivo study in rabbits. J Oral Maxillofac Surg 64:1005–1009CrossRefPubMed
24.
Zurück zum Zitat Narai S, Nagahata S (2003) Effects of alendronate on the removal torque of implants in rats with induced osteoporosis. Int J Oral Maxillofac Implants 18:218–223PubMed Narai S, Nagahata S (2003) Effects of alendronate on the removal torque of implants in rats with induced osteoporosis. Int J Oral Maxillofac Implants 18:218–223PubMed
25.
Zurück zum Zitat Guimaraes MB, Bueno RS, Blaya MB, Shinkai RS, Marques LM (2015) Influence of the local application of sodium alendronate gel on osseointegration of titanium implants. Int J Oral Maxillofac Surg 44:1423–1429CrossRefPubMed Guimaraes MB, Bueno RS, Blaya MB, Shinkai RS, Marques LM (2015) Influence of the local application of sodium alendronate gel on osseointegration of titanium implants. Int J Oral Maxillofac Surg 44:1423–1429CrossRefPubMed
26.
Zurück zum Zitat Fuchs RK, Phipps RJ, Burr DB (2008) Recovery of trabecular and cortical bone turnover after discontinuation of risedronate and alendronate therapy in ovariectomized rats. J Bone Miner Res 23:1689–1697CrossRefPubMedPubMedCentral Fuchs RK, Phipps RJ, Burr DB (2008) Recovery of trabecular and cortical bone turnover after discontinuation of risedronate and alendronate therapy in ovariectomized rats. J Bone Miner Res 23:1689–1697CrossRefPubMedPubMedCentral
27.
Zurück zum Zitat Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2012) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Osteoarthr Cartil 20:256–260CrossRef Kilkenny C, Browne WJ, Cuthill IC, Emerson M, Altman DG (2012) Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Osteoarthr Cartil 20:256–260CrossRef
28.
Zurück zum Zitat de Molon RS, Morais-Camilo JA, Verzola MH, Faeda RS, Pepato MT, Marcantonio E Jr (2013) Impact of diabetes mellitus and metabolic control on bone healing around osseointegrated implants: removal torque and histomorphometric analysis in rats. Clin Oral Implants Res 24:831–837CrossRefPubMed de Molon RS, Morais-Camilo JA, Verzola MH, Faeda RS, Pepato MT, Marcantonio E Jr (2013) Impact of diabetes mellitus and metabolic control on bone healing around osseointegrated implants: removal torque and histomorphometric analysis in rats. Clin Oral Implants Res 24:831–837CrossRefPubMed
29.
Zurück zum Zitat Dos Santos PL, de Molon RS, Queiroz TP, Okamoto R, de Souza Faloni AP, Gulinelli JL, Luvizuto ER, Garcia IR Jr (2016) Evaluation of bone substitutes for treatment of peri-implant bone defects: biomechanical, histological, and immunohistochemical analyses in the rabbit tibia. J Periodontal Implant Sci 46:176–196CrossRefPubMedPubMedCentral Dos Santos PL, de Molon RS, Queiroz TP, Okamoto R, de Souza Faloni AP, Gulinelli JL, Luvizuto ER, Garcia IR Jr (2016) Evaluation of bone substitutes for treatment of peri-implant bone defects: biomechanical, histological, and immunohistochemical analyses in the rabbit tibia. J Periodontal Implant Sci 46:176–196CrossRefPubMedPubMedCentral
30.
Zurück zum Zitat Kim YJ, de Molon RR, Horiguti FR, Contador GP, Coelho MA, Mascarenhas VI, de Souza Faloni AP, Cirelli JA, Sendyk WR (2018) Vertical bone augmentation using Deproteinized bovine bone mineral, absorbable collagen sponge, and recombinant human bone morphogenetic Protein-2: an in vivo study in rabbits. Int J Oral Maxillofac Implants, 33, 512, 522 Kim YJ, de Molon RR, Horiguti FR, Contador GP, Coelho MA, Mascarenhas VI, de Souza Faloni AP, Cirelli JA, Sendyk WR (2018) Vertical bone augmentation using Deproteinized bovine bone mineral, absorbable collagen sponge, and recombinant human bone morphogenetic Protein-2: an in vivo study in rabbits. Int J Oral Maxillofac Implants, 33, 512, 522
31.
Zurück zum Zitat Queiroz TP, de Molon RS, Souza FA, Margonar R, Thomazini AH, Guastaldi AC, Hochuli-Vieira E (2017) In vivo evaluation of cp Ti implants with modified surfaces by laser beam with and without hydroxyapatite chemical deposition and without and with thermal treatment: topographic characterization and histomorphometric analysis in rabbits. Clin Oral Investig 21:685–699CrossRefPubMed Queiroz TP, de Molon RS, Souza FA, Margonar R, Thomazini AH, Guastaldi AC, Hochuli-Vieira E (2017) In vivo evaluation of cp Ti implants with modified surfaces by laser beam with and without hydroxyapatite chemical deposition and without and with thermal treatment: topographic characterization and histomorphometric analysis in rabbits. Clin Oral Investig 21:685–699CrossRefPubMed
32.
Zurück zum Zitat Vidigal GM Jr, Aragones LC, Campos A Jr, Groisman M (1999) Histomorphometric analyses of hydroxyapatite-coated and uncoated titanium dental implants in rabbit cortical bone. Implant Dent 8:295–302CrossRefPubMed Vidigal GM Jr, Aragones LC, Campos A Jr, Groisman M (1999) Histomorphometric analyses of hydroxyapatite-coated and uncoated titanium dental implants in rabbit cortical bone. Implant Dent 8:295–302CrossRefPubMed
33.
Zurück zum Zitat Zagury R, Harari ND, Conz MB, Soares Gde A, Vidigal GM Jr (2007) Histomorphometric analyses of bone interface with titanium-aluminum-vanadium and hydroxyapatite-coated implants by biomimetic process. Implant Dent 16:290–296CrossRefPubMed Zagury R, Harari ND, Conz MB, Soares Gde A, Vidigal GM Jr (2007) Histomorphometric analyses of bone interface with titanium-aluminum-vanadium and hydroxyapatite-coated implants by biomimetic process. Implant Dent 16:290–296CrossRefPubMed
35.
Zurück zum Zitat Yildiz A, Esen E, Kurkcu M, Damlar I, Daglioglu K, Akova T (2010) Effect of zoledronic acid on osseointegration of titanium implants: an experimental study in an ovariectomized rabbit model. J Oral Maxillofac Surg 68:515–523CrossRefPubMed Yildiz A, Esen E, Kurkcu M, Damlar I, Daglioglu K, Akova T (2010) Effect of zoledronic acid on osseointegration of titanium implants: an experimental study in an ovariectomized rabbit model. J Oral Maxillofac Surg 68:515–523CrossRefPubMed
36.
Zurück zum Zitat Silva AG, Vieira JG, Kunii IS, Lana JM, Lazaretti-Castro M (2011) The effects of discontinuing long term alendronate therapy in a clinical practice setting. Arq Bras Endocrinol Metabol 55:272–278CrossRefPubMed Silva AG, Vieira JG, Kunii IS, Lana JM, Lazaretti-Castro M (2011) The effects of discontinuing long term alendronate therapy in a clinical practice setting. Arq Bras Endocrinol Metabol 55:272–278CrossRefPubMed
37.
Zurück zum Zitat Wasnich RD, Bagger YZ, Hosking DJ, McClung MR, Wu M, Mantz AM, Yates JJ, Ross PD, Alexandersen P, Ravn P, Christiansen C, Santora AC, 2nd, Early Postmenopausal Intervention Cohort Study G (2004) Changes in bone density and turnover after alendronate or estrogen withdrawal. Menopause 11:622–630 Wasnich RD, Bagger YZ, Hosking DJ, McClung MR, Wu M, Mantz AM, Yates JJ, Ross PD, Alexandersen P, Ravn P, Christiansen C, Santora AC, 2nd, Early Postmenopausal Intervention Cohort Study G (2004) Changes in bone density and turnover after alendronate or estrogen withdrawal. Menopause 11:622–630
38.
Zurück zum Zitat Black DM, Cummings SR, Karpf DB, Cauley JA, Thompson DE, Nevitt MC, Bauer DC, Genant HK, Haskell WL, Marcus R, Ott SM, Torner JC, Quandt SA, Reiss TF, Ensrud KE (1996) Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group. Lancet 348:1535–1541CrossRefPubMed Black DM, Cummings SR, Karpf DB, Cauley JA, Thompson DE, Nevitt MC, Bauer DC, Genant HK, Haskell WL, Marcus R, Ott SM, Torner JC, Quandt SA, Reiss TF, Ensrud KE (1996) Randomised trial of effect of alendronate on risk of fracture in women with existing vertebral fractures. Fracture Intervention Trial Research Group. Lancet 348:1535–1541CrossRefPubMed
39.
Zurück zum Zitat Black DM, Reid IR, Boonen S, Bucci-Rechtweg C, Cauley JA, Cosman F, Cummings SR, Hue TF, Lippuner K, Lakatos P, Leung PC, Man Z, Martinez RL, Tan M, Ruzycky ME, Su G, Eastell R (2012) The effect of 3 versus 6 years of zoledronic acid treatment of osteoporosis: a randomized extension to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 27:243–254CrossRefPubMed Black DM, Reid IR, Boonen S, Bucci-Rechtweg C, Cauley JA, Cosman F, Cummings SR, Hue TF, Lippuner K, Lakatos P, Leung PC, Man Z, Martinez RL, Tan M, Ruzycky ME, Su G, Eastell R (2012) The effect of 3 versus 6 years of zoledronic acid treatment of osteoporosis: a randomized extension to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 27:243–254CrossRefPubMed
40.
Zurück zum Zitat Black DM, Reid IR, Cauley JA, Cosman F, Leung PC, Lakatos P, Lippuner K, Cummings SR, Hue TF, Mukhopadhyay A, Tan M, Aftring RP, Eastell R (2015) The effect of 6 versus 9 years of zoledronic acid treatment in osteoporosis: a randomized second extension to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 30:934–944CrossRefPubMed Black DM, Reid IR, Cauley JA, Cosman F, Leung PC, Lakatos P, Lippuner K, Cummings SR, Hue TF, Mukhopadhyay A, Tan M, Aftring RP, Eastell R (2015) The effect of 6 versus 9 years of zoledronic acid treatment in osteoporosis: a randomized second extension to the HORIZON-Pivotal Fracture Trial (PFT). J Bone Miner Res 30:934–944CrossRefPubMed
41.
Zurück zum Zitat Shahnazari M, Yao W, Wang B, Panganiban B, Ritchie RO, Hagar Y, Lane NE (2011) Differential maintenance of cortical and cancellous bone strength following discontinuation of bone-active agents. J Bone Miner Res 26:569–581CrossRefPubMed Shahnazari M, Yao W, Wang B, Panganiban B, Ritchie RO, Hagar Y, Lane NE (2011) Differential maintenance of cortical and cancellous bone strength following discontinuation of bone-active agents. J Bone Miner Res 26:569–581CrossRefPubMed
42.
Zurück zum Zitat Bagger YZ, Tanko LB, Alexandersen P, Ravn P, Christiansen C (2003) Alendronate has a residual effect on bone mass in postmenopausal Danish women up to 7 years after treatment withdrawal. Bone 33:301–307CrossRefPubMed Bagger YZ, Tanko LB, Alexandersen P, Ravn P, Christiansen C (2003) Alendronate has a residual effect on bone mass in postmenopausal Danish women up to 7 years after treatment withdrawal. Bone 33:301–307CrossRefPubMed
43.
Zurück zum Zitat Grey A, Bolland M, Wattie D, Horne A, Gamble G, Reid IR (2010) Prolonged antiresorptive activity of zoledronate: a randomized controlled trial. J Bone Miner Res 25:2251–2255CrossRefPubMed Grey A, Bolland M, Wattie D, Horne A, Gamble G, Reid IR (2010) Prolonged antiresorptive activity of zoledronate: a randomized controlled trial. J Bone Miner Res 25:2251–2255CrossRefPubMed
44.
Zurück zum Zitat Manzano-Moreno FJ, Ramos-Torrecillas J, De Luna-Bertos E, Reyes-Botella C, Ruiz C, Garcia-Martinez O (2015) Nitrogen-containing bisphosphonates modulate the antigenic profile and inhibit the maturation and biomineralization potential of osteoblast-like cells. Clin Oral Investig 19:895–902 Manzano-Moreno FJ, Ramos-Torrecillas J, De Luna-Bertos E, Reyes-Botella C, Ruiz C, Garcia-Martinez O (2015) Nitrogen-containing bisphosphonates modulate the antigenic profile and inhibit the maturation and biomineralization potential of osteoblast-like cells. Clin Oral Investig 19:895–902
45.
Zurück zum Zitat Chen JT, Hosoda K, Hasumi K, Ogata E, Shiraki M (1996) Serum N-terminal osteocalcin is a good indicator for estimating responders to hormone replacement therapy in postmenopausal women. J Bone Miner Res 11:1784–1792CrossRefPubMed Chen JT, Hosoda K, Hasumi K, Ogata E, Shiraki M (1996) Serum N-terminal osteocalcin is a good indicator for estimating responders to hormone replacement therapy in postmenopausal women. J Bone Miner Res 11:1784–1792CrossRefPubMed
46.
Zurück zum Zitat Wolf G (1996) Function of the bone protein osteocalcin: definitive evidence. Nutr Rev 54:332–333CrossRefPubMed Wolf G (1996) Function of the bone protein osteocalcin: definitive evidence. Nutr Rev 54:332–333CrossRefPubMed
47.
Zurück zum Zitat Black DM, Schwartz AV, Ensrud KE, Cauley JA, Levis S, Quandt SA, Satterfield S, Wallace RB, Bauer DC, Palermo L, Wehren LE, Lombardi A, Santora AC, Cummings SR, Group FR (2006) Effects of continuing or stopping alendronate after 5 years of treatment: the fracture intervention trial long-term extension (FLEX): a randomized trial. JAMA 296:2927–2938CrossRefPubMed Black DM, Schwartz AV, Ensrud KE, Cauley JA, Levis S, Quandt SA, Satterfield S, Wallace RB, Bauer DC, Palermo L, Wehren LE, Lombardi A, Santora AC, Cummings SR, Group FR (2006) Effects of continuing or stopping alendronate after 5 years of treatment: the fracture intervention trial long-term extension (FLEX): a randomized trial. JAMA 296:2927–2938CrossRefPubMed
48.
Zurück zum Zitat Ensrud KE, Barrett-Connor EL, Schwartz A, Santora AC, Bauer DC, Suryawanshi S, Feldstein A, Haskell WL, Hochberg MC, Torner JC, Lombardi A, Black DM, Fracture Intervention Trial Long-Term Extension Research G (2004) Randomized trial of effect of alendronate continuation versus discontinuation in women with low BMD: results from the fracture intervention trial long-term extension. J Bone Miner Res 19:1259–1269CrossRefPubMed Ensrud KE, Barrett-Connor EL, Schwartz A, Santora AC, Bauer DC, Suryawanshi S, Feldstein A, Haskell WL, Hochberg MC, Torner JC, Lombardi A, Black DM, Fracture Intervention Trial Long-Term Extension Research G (2004) Randomized trial of effect of alendronate continuation versus discontinuation in women with low BMD: results from the fracture intervention trial long-term extension. J Bone Miner Res 19:1259–1269CrossRefPubMed
49.
Zurück zum Zitat Tamura Y, Miyakoshi N, Itoi E, Abe T, Kudo T, Tsuchida T, Kasukawa Y, Sato K (2001) Long-term effects of withdrawal of bisphosphonate incadronate disodium (YM175) on bone mineral density, mass, structure, and turnover in the lumbar vertebrae of ovariectomized rats. J Bone Miner Res 16:541–549CrossRefPubMed Tamura Y, Miyakoshi N, Itoi E, Abe T, Kudo T, Tsuchida T, Kasukawa Y, Sato K (2001) Long-term effects of withdrawal of bisphosphonate incadronate disodium (YM175) on bone mineral density, mass, structure, and turnover in the lumbar vertebrae of ovariectomized rats. J Bone Miner Res 16:541–549CrossRefPubMed
50.
Zurück zum Zitat Duarte PM, de Vasconcelos Gurgel BC, Sallum AW, Filho GR, Sallum EA, Nociti FH Jr (2005) Alendronate therapy may be effective in the prevention of bone loss around titanium implants inserted in estrogen-deficient rats. J Periodontol 76:107–114CrossRefPubMed Duarte PM, de Vasconcelos Gurgel BC, Sallum AW, Filho GR, Sallum EA, Nociti FH Jr (2005) Alendronate therapy may be effective in the prevention of bone loss around titanium implants inserted in estrogen-deficient rats. J Periodontol 76:107–114CrossRefPubMed
51.
Zurück zum Zitat Mardas N, Schwarz F, Petrie A, Hakimi AR, Donos N (2011) The effect of SLActive surface in guided bone formation in osteoporotic-like conditions. Clin Oral Implants Res 22:406–415CrossRefPubMed Mardas N, Schwarz F, Petrie A, Hakimi AR, Donos N (2011) The effect of SLActive surface in guided bone formation in osteoporotic-like conditions. Clin Oral Implants Res 22:406–415CrossRefPubMed
52.
Zurück zum Zitat Komatsubara S, Mori S, Mashiba T, Li J, Nonaka K, Kaji Y, Akiyama T, Miyamoto K, Cao Y, Kawanishi J, Norimatsu H (2004) Suppressed bone turnover by long-term bisphosphonate treatment accumulates microdamage but maintains intrinsic material properties in cortical bone of dog rib. J Bone Miner Res 19:999–1005CrossRefPubMed Komatsubara S, Mori S, Mashiba T, Li J, Nonaka K, Kaji Y, Akiyama T, Miyamoto K, Cao Y, Kawanishi J, Norimatsu H (2004) Suppressed bone turnover by long-term bisphosphonate treatment accumulates microdamage but maintains intrinsic material properties in cortical bone of dog rib. J Bone Miner Res 19:999–1005CrossRefPubMed
53.
Zurück zum Zitat Berglundh T, Abrahamsson I, Lang NP, Lindhe J (2003) De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 14:251–262CrossRefPubMed Berglundh T, Abrahamsson I, Lang NP, Lindhe J (2003) De novo alveolar bone formation adjacent to endosseous implants. Clin Oral Implants Res 14:251–262CrossRefPubMed
54.
Zurück zum Zitat Russell RG, Watts NB, Ebetino FH, Rogers MJ (2008) Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int 19:733–759CrossRefPubMed Russell RG, Watts NB, Ebetino FH, Rogers MJ (2008) Mechanisms of action of bisphosphonates: similarities and differences and their potential influence on clinical efficacy. Osteoporos Int 19:733–759CrossRefPubMed
55.
Zurück zum Zitat Yip JK, Borrell LN, Cho SC, Francisco H, Tarnow DP (2012) Association between oral bisphosphonate use and dental implant failure among middle-aged women. J Clin Periodontol 39:408–414CrossRefPubMed Yip JK, Borrell LN, Cho SC, Francisco H, Tarnow DP (2012) Association between oral bisphosphonate use and dental implant failure among middle-aged women. J Clin Periodontol 39:408–414CrossRefPubMed
56.
Zurück zum Zitat Bedogni A, Bettini G, Totola A, Saia G, Nocini PF (2010) Oral bisphosphonate-associated osteonecrosis of the jaw after implant surgery: a case report and literature review. J Oral Maxillofac Surg 68:1662–1666CrossRefPubMed Bedogni A, Bettini G, Totola A, Saia G, Nocini PF (2010) Oral bisphosphonate-associated osteonecrosis of the jaw after implant surgery: a case report and literature review. J Oral Maxillofac Surg 68:1662–1666CrossRefPubMed
57.
Zurück zum Zitat Starck WJ, Epker BN (1995) Failure of osseointegrated dental implants after diphosphonate therapy for osteoporosis: a case report. Int J Oral Maxillofac Implants 10:74–78PubMed Starck WJ, Epker BN (1995) Failure of osseointegrated dental implants after diphosphonate therapy for osteoporosis: a case report. Int J Oral Maxillofac Implants 10:74–78PubMed
58.
Zurück zum Zitat Yuan K, Chen KC, Chan YJ, Tsai CC, Chen HH, Shih CC (2012) Dental implant failure associated with bacterial infection and long-term bisphosphonate usage: a case report. Implant Dent 21:3–7CrossRefPubMed Yuan K, Chen KC, Chan YJ, Tsai CC, Chen HH, Shih CC (2012) Dental implant failure associated with bacterial infection and long-term bisphosphonate usage: a case report. Implant Dent 21:3–7CrossRefPubMed
59.
Zurück zum Zitat de Molon RS, Cheong S, Bezouglaia O, Dry SM, Pirih F, Cirelli JA, Aghaloo TL, Tetradis S (2014) Spontaneous osteonecrosis of the jaws in the maxilla of mice on antiresorptive treatment: a novel ONJ mouse model. Bone 68:11–19CrossRefPubMedPubMedCentral de Molon RS, Cheong S, Bezouglaia O, Dry SM, Pirih F, Cirelli JA, Aghaloo TL, Tetradis S (2014) Spontaneous osteonecrosis of the jaws in the maxilla of mice on antiresorptive treatment: a novel ONJ mouse model. Bone 68:11–19CrossRefPubMedPubMedCentral
60.
Zurück zum Zitat de Molon RS, Hsu C, Bezouglaia O, Dry SM, Pirih FQ, Soundia A, Cunha FQ, Cirelli JA, Aghaloo TL, Tetradis S (2016) Rheumatoid arthritis exacerbates the severity of osteonecrosis of the jaws (ONJ) in mice. A randomized, prospective, controlled animal study. J Bone Miner Res 31:1596–1607CrossRefPubMed de Molon RS, Hsu C, Bezouglaia O, Dry SM, Pirih FQ, Soundia A, Cunha FQ, Cirelli JA, Aghaloo TL, Tetradis S (2016) Rheumatoid arthritis exacerbates the severity of osteonecrosis of the jaws (ONJ) in mice. A randomized, prospective, controlled animal study. J Bone Miner Res 31:1596–1607CrossRefPubMed
61.
Zurück zum Zitat de Molon RS, Shimamoto H, Bezouglaia O, Pirih FQ, Dry SM, Kostenuik P, Boyce RW, Dwyer D, Aghaloo TL, Tetradis S (2015) OPG-fc but not Zoledronic acid discontinuation reverses osteonecrosis of the jaws (ONJ) in mice. J Bone Miner Res 30:1627–1640CrossRefPubMed de Molon RS, Shimamoto H, Bezouglaia O, Pirih FQ, Dry SM, Kostenuik P, Boyce RW, Dwyer D, Aghaloo TL, Tetradis S (2015) OPG-fc but not Zoledronic acid discontinuation reverses osteonecrosis of the jaws (ONJ) in mice. J Bone Miner Res 30:1627–1640CrossRefPubMed
Metadaten
Titel
Evaluation of bone turnover after bisphosphonate withdrawal and its influence on implant osseointegration: an in vivo study in rats
verfasst von
Fausto Frizzera
Mario Henrique Arruda Verzola
Rafael Scaf de Molon
Guilherme Jose Pimentel Lopes de Oliveira
Gabriela Giro
Luis Carlos Spolidorio
Rosa Maria Rodrigues Pereira
Sotirios Tetradis
Joni Augusto Cirelli
Silvana Regina Peres Orrico
Publikationsdatum
30.08.2018
Verlag
Springer Berlin Heidelberg
Erschienen in
Clinical Oral Investigations / Ausgabe 4/2019
Print ISSN: 1432-6981
Elektronische ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-018-2612-x

Weitere Artikel der Ausgabe 4/2019

Clinical Oral Investigations 4/2019 Zur Ausgabe

Newsletter

Bestellen Sie unseren kostenlosen Newsletter Update Zahnmedizin und bleiben Sie gut informiert – ganz bequem per eMail.