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Effects of Pamidronate on Dental Enamel Formation Assessed by Light Microscopy, Energy-Dispersive X-Ray Analysis, Scanning Electron Microscopy, and Microhardness Testing

Published online by Cambridge University Press:  23 May 2016

Ana P. Soares ,
Renan F. do Espírito Santo ,
Sérgio R. P. Line ,
Maria das G. F. Pinto ,
Pablo de M. Santos ,
Maria Betania P. Toralles  and
Alexandre R. do Espírito Santo
Ana P. Soares
Affiliation:
Multidisciplinary Institute of Health, Federal University of Bahia—UFBA, Rua Rio de Contas, 58, Quadra 17, Lote 58, Candeias, Vitória da Conquista, BA CEP 45.029-094, Brasil
Renan F. do Espírito Santo
Affiliation:
Faculty of Pharmacy, Federal University of Bahia—UFBA, Rua Barão de Jeremoabo, S/N, Campus Universitário de Ondina, Ondina, Salvador, BA CEP 40.170-115, Brasil
Sérgio R. P. Line
Affiliation:
Piracicaba Dental School, University of Campinas—UNICAMP, Av. Limeira, 901, Areião, Piracicaba, SP CEP 13.414-903, Brasil
Maria das G. F. Pinto
Affiliation:
School of Veterinary Medicine and Zootechny, Federal University of Bahia—UFBA, Av. Ademar de Barros, 500, Ondina, Salvador, BA CEP 40.170-110, Brasil
Pablo de M. Santos
Affiliation:
Professor Edgard Santos University Hospital, Federal University of Bahia—UFBA, Rua Augusto Viana, S/N, Canela, Salvador, BA CEP 40.110-060, Brasil
Maria Betania P. Toralles
Affiliation:
Institute of Health Sciences, Federal University of Bahia—UFBA, Av. Reitor Miguel Calmon, S/N, Vale do Canela, Salvador, BA CEP 40.110-902, Brasil
Alexandre R. do Espírito Santo*
Affiliation:
Institute of Health Sciences, Federal University of Bahia—UFBA, Av. Reitor Miguel Calmon, S/N, Vale do Canela, Salvador, BA CEP 40.110-902, Brasil
*
*Corresponding author. arespiritosanto@ufba.br
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Abstract

The aim of the present work was to investigate birefringence and morphology of the secretory-stage enamel organic extracellular matrix (EOECM), and structural and mechanical properties of mature enamel of upper incisors from adult rats that had been treated with pamidronate disodium (0.5 mg/kg/week for 56 days), using transmitted polarizing and bright-field light microscopies (TPLM and BFLM), energy-dispersive X-ray (EDX) analysis, scanning electron microscopy (SEM) and microhardness testing. BFLM showed no morphological changes of the EOECM in pamidronate and control groups, but TPLM revealed a statistically significant reduction in optical retardation values of birefringence brightness of pamidronate-treated rats when compared with control animals (p<0.01). EDX analysis showed that pamidronate-induced statistically significant decrease in phosphorus’ quantity in outer mature enamel (p<0.01) and an increase in the calcium/phosphorus ratio in that structure (p<0.05). Pamidronate did not induce ultra-structural alterations in mature enamel as revealed by SEM and did not cause a reduction in its microhardness (p>0.05). The present study indicates that pamidronate can affect birefringence of the secretory-stage EOECM, which does not seem to be associated with significant changes in morphological and/or mechanical properties of mature enamel.

Keywords

bisphosphonatesenamellight microscopyscanning electron microscopymicroanalysis
Type
Biological Applications
Information
Microscopy and Microanalysis , Volume 22 , Issue 3 , June 2016 , pp. 640 - 648
Copyright
Copyright © Microscopy Society of America 2016

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References

August, K.J., Dalton, A., Katzenstein, H.M., George, B., Olson, T.A., Wasilewski-Masker, K. & Rapkin, L.B. (2011). The use of zoledronic acid in pediatric cancer patients. Pediatr Blood Cancer 56, 610–614.Google Scholar
Bachrach, L.K. & Ward, L.M. (2009). Clinical review 1: Bisphosphonate use in childhood osteoporosis. J Clin Endocrinol Metab 94, 400–409.10.1210/jc.2008-1531Google Scholar
Bajpai, A., Kabra, M., Gupta, N., Sharda, S. & Ghosh, M. (2007). Intravenous pamidronate therapy in osteogenesis imperfecta: Response to treatment and factors influencing outcome. J Pediatr Orthop 27, 225–227.10.1097/bpo.0b013e3180316d06Google Scholar
Baroncelli, G.I. & Bertelloni, S. (2014). The use of bisphosphonates in pediatrics. Horm Res Paediatr 82, 290–302.Google Scholar
Barros, E.R., Saraiva, G.L., de Oliveira, T.P. & Lazaretti-Castro, M. (2012). Safety and efficacy of a 1-year treatment with zoledronic acid compared with pamidronate in children with osteogenesis imperfecta. J Pediatr Endocrinol Metab 25, 485–491.Google Scholar
Bartlett, J.D. (2013). Dental enamel development: Proteinases and their enamel matrix substrates. ISRN Dent 2013, PMC3789414.Google Scholar
Bishop, N., Adami, S., Ahmed, S.F., Antón, J., Arundel, P., Burren, C.P., Devogelaer, J.P., Hangartner, T., Hosszú, E., Lane, J.M., Lorenc, R., Mäkitie, O., Munns, C.F., Paredes, A., Pavlov, H., Plotkin, H., Raggio, C.L., Reyes, M.L., Schoenau, E., Semler, O., Sillence, D.O. & Steiner, R.D. (2013). Risedronate in children with osteogenesis imperfecta: A randomised, double-blind, placebo-controlled trial. Lancet 382, 1424–1432.Google Scholar
Castillo, H. & Samson-Fang, L. & American Academy for Cerebral Palsy and Developmental Medicine Treatment Outcomes Committee Review Panel (2009). Effects of bisphosphonates in children with osteogenesis imperfecta: An AACPDM systematic review. Dev Med Child Neurol 51, 17–29.Google Scholar
Chilbule, S.K. & Madhuri, V. (2012). Complications of pamidronate therapy in paediatric osteoporosis. J Child Orthop 6, 37–43.10.1007/s11832-012-0383-5Google Scholar
Cremers, S. & Papapoulos, S. (2011). Pharmacology of bisphosphonates. Bone 49, 42–49.10.1016/j.bone.2011.01.014Google Scholar
do Espírito Santo, A.R., Frozoni, M.R., Ramos-Perez, F.M., Novaes, P.D. & Line, S.R. (2010). Birefringence of the secretory-stage enamel organic extracellular matrix from rats submitted to successive injections of bisphosphonates. Connect Tissue Res 51, 208–215.10.3109/03008200903280115Google Scholar
do Espírito Santo, A.R., Novaes, P.D. & Line, S.R. (2006). Anisotropic properties of the enamel organic extracellular matrix. Eur J Oral Sci 114(Suppl 1), 333–337.Google Scholar
Dwan, K., Phillipi, C.A., Steiner, R.D. & Basel, D. (2014). Bisphosphonate therapy for osteogenesis imperfecta. Cochrane Database Syst Rev 7, CD005088. doi: 10.1002/14651858.CD005088.pub3.Google Scholar
Espírito Santo, A.R., Bartlett, J.D., Gibson, C.W., Li, Y., Kulkarni, A.B. & Line, S.R. (2007). Amelogenin- and enamelysin (Mmp-20)-deficient mice display altered birefringence in the secretory-stage enamel organic extracellular matrix. Connect Tissue Res 48, 39–45.Google Scholar
Fejerskov, O., Josephsen, K. & Weile, V. (1990). The effect of a single dose of 1-hydroxyethylidene-1, 1-bisphosphonate (HEBP) on secretory ameloblasts and enamel formation in rat incisors. J Biol Buccale 18, 339–354.Google Scholar
Fleisch, H. (1993). Prospective use of bisphosphonates in osteoporosis. J Clin Endocrinol Metab 76, 1397–1398.Google Scholar
Fleisch, H. (1997). Bisphosphonates: Mechanisms of action and clinical use in osteoporosis—an update. Horm Metab Res 29, 145–150.Google Scholar
Fouda, N., Caracatsanis, M. & Hammarstrom, L. (1989). Developmental disturbances of the rat molar induced by two diphosphonates. Adv Dent Res 3, 234–240.10.1177/08959374890030022401Google Scholar
Fouda, N., Caracatsanis, M., Kut, I.A. & Hammarstrom, L. (1991). Mineralization disturbances of the developing rat molar induced by mono- and bisphosphonates. J Biol Buccale 19, 106–115.Google Scholar
Fuangtharnthip, P., Yamada, Y., Takagi, Y. & Ohya, K. (2000). Autoradiographic investigation of the effect of 1-hydroxyethylidene, 1-bisphosphonate on matrix protein synthesis and secretion by secretory ameloblasts in rat incisors. Arch Oral Biol 45, 495–506.10.1016/S0003-9969(00)00009-1Google Scholar
Glorieux, F.H., Bishop, N.J., Plotkin, H., Chabot, G., Lanoue, G. & Travers, R. (1998). Cyclic administration of pamidronate in children with severe osteogenesis imperfecta. N Engl J Med 339, 947–952.10.1056/NEJM199810013391402Google Scholar
Heikkilä, P., Teronen, O., Moilanen, M., Konttinen, Y.T., Hanemaaijer, R., Laitinen, M., Maisi, P., van der Pluijm, G., Bartlett, J.D., Salo, T. & Sorsa, T. (2002). Bisphosphonates inhibit stromelysin-1 (MMP-3), matrix metalloelastase (MMP-12), collagenase-3 (MMP-13) and enamelysin (MMP-20), but not urokinase-type plasminogen activator, and diminish invasion and migration of human malignant and endothelial cell lines. Anticancer Drugs 13, 245–254.10.1097/00001813-200203000-00006Google Scholar
Hiraga, T., Ninomiya, T., Hosoya, A. & Nakamura, H. (2010). Administration of the bisphosphonate zoledronic acid during tooth development inhibits tooth eruption and formation and induces dental abnormalities in rats. Calcif Tissue Int 86, 502–510.10.1007/s00223-010-9366-zGoogle Scholar
Iwai, T., Isomatsu, Y., Iwamoto, M. & Tohnai, I. (2013). Bisphosphonate-related enamel hypoplasia in a child with idiopathic arterial calcification of infancy. Br J Oral Maxillofac Surg 51, e186–e187.Google Scholar
Josephsen, K., Fejerskov, O., Baelum, V. & Weile, V. (1990). The effect of a single dose of 1-hydroxyethylidene-1,1-bisphosphonate (HEBP) on presecretory ameloblast differentiation in rat incisors. J Biol Buccale 18, 321–337.Google Scholar
Kamoun-Goldrat, A., Ginisty, D. & Le Merrer, M. (2008). Effects of bisphosphonates on tooth eruption in children with osteogenesis imperfecta. Eur J Oral Sci 116, 195–198.10.1111/j.1600-0722.2008.00529.xGoogle Scholar
Kitaoka, T., Namba, N., Miura, K., Kubota, T., Ohata, Y., Fujiwara, M., Hirai, H., Yamamoto, T. & Ozono, K. (2011). Decrease in serum FGF23 levels after intravenous infusion of pamidronate in patients with osteogenesis imperfecta. J Bone Miner Metab 29, 598–605.Google Scholar
Maasalu, K., Haviko, T. & Martson, A. (2003). Treatment of children with osteogenesis imperfecta in Estonia. Acta Paediatr 92, 452–455.10.1111/j.1651-2227.2003.tb00577.xGoogle Scholar
Massa, L.F., Bradaschia-Correa, V. & Arana-Chavez, V.E. (2006). Immunocytochemical study of amelogenin deposition during the early odontogenesis of molars in alendronate-treated newborn rats. J Histochem Cytochem 54, 713–725.10.1369/jhc.5A6853.2006Google Scholar
Modesto, A., Klein, O., Tenuta, L.M., Gerlach, R.F. & Vieira, A.R. (2013). Summary of the IADR Cariology Research, Craniofacial Biology, and Mineralized Tissue Groups Symposium, Iguaçu Falls, Brazil, June 2012: Gene-environment interactions and epigenetics in oral diseases: enamel formation and its clinical impact on tooth defects, caries, and erosion. Dent 3000 1, PMC4225817.Google Scholar
Nelson-Filho, P., Lucisano, M.P., da Silva, R.A., da Silva, R.S., Serra, M.C., Gerlach, R.F., Neto, F.C., Carneiro, Z.A., Zamarioli, A., Morse, L. & Battaglino, R. (2012). Systemically alendronate was incorporated into dental tissues but did not cause morphological or mechanical changes in rats teeth. Microsc Res Tech 75, 1265–1271.10.1002/jemt.22059Google Scholar
Phillipi, C.A., Remmington, T. & Steiner, R.D. (2008). Bisphosphonate therapy for osteogenesis imperfecta. Cochrane Database Syst Rev 4, CD005088. doi: 10.1002/14651858.CD005088.pub2.Google Scholar
Plotkin, H., Rauch, F., Bishop, N.J., Montpetit, K., Ruck-Gibis, J., Travers, R. & Glorieux, F.H. (2000). Pamidronate treatment of severe osteogenesis imperfecta in children under 3 years of age. J Clin Endocrinol Metab 85, 1846–1850.Google Scholar
Rodan, G.A. & Fleisch, H.A. (1996). Bisphosphonates: Mechanisms of action. J Clin Invest 97, 2692–2696.Google Scholar
Russell, R.G. (2011). Bisphosphonates: The first 40 years. Bone 49, 2–19.Google Scholar
Simmelink, J.W. (1987). Ultrastructural effects of diphosphonates on dental enamel. Adv Dent Res 1, 356–365.10.1177/08959374870010022701Google Scholar
Smith, C.E. & Nanci, A. (1989). A method for sampling the stages of amelogenesis on mandibular rat incisors using the molars as a reference for dissection. Anat Rec 225, 257–266.10.1002/ar.1092250312Google Scholar
Sukumar, S.P., Balachandran, K., Sahoo, J.P. & Kamalanathan, S. (2013). Zebra lines in osteogenesis imperfecta on bisphosphonate therapy. BMJ Case Rep 2013, 1–2.10.1136/bcr-2012-008536Google Scholar
Thesleff, I., Vaahtokari, A., Kettunen, P. & Aberg, T. (1995). Epithelial-mesenchymal signaling during tooth development. Connect Tissue Res 32, 9–15.Google Scholar
van Beek, E.R., Lowik, C. & Papapoulos, S. (2002). Bisphosphonates suppress bone resorption by a direct effect on early osteoclast precursors without affecting the osteoclastogenic capacity of osteogenic cells: The role of protein geranylgeranylation in the action of nitrogen-containing bisphosphonates on osteoclast precursors. Bone 30, 64–70.10.1016/S8756-3282(01)00655-XGoogle Scholar
van Beek, E.R., Pieterman, E., Cohen, L., Lowik, C. & Papapoulos, S. (1999). Nitrogen-containing bisphosphonates inhibit isopentenyl pyrophosphate isomerase/farnesyl pyrophosphate synthase activity with relative potencies corresponding to their antiresorptive pontencies in vitro and in vivo. Biochem Biophys Res Commun 263, 754–758.Google Scholar
Wakamatsu, H. (1991). A study of the effects of successive injections of 1-hydroxyethylidene-1, 1-bisphosphonate (HEBP) on the enamel formation of rat incisor. Jpn J Oral Biol 33, 82–96.Google Scholar
Ward, L.M., Rauch, F., Whyte, M.P., D’Astous, J., Gates, P.E., Grogan, D., Lester, E.L., McCall, R.E., Pressly, T.A., Sanders, J.O., Smith, P.A., Steiner, R.D., Sullivan, E., Tyerman, G., Smith-Wright, D.L., Verbruggen, N., Heyden, N., Lombardi, A. & Glorieux, F.H. (2011). Alendronate for the treatment of pediatric osteogenesis imperfecta: A randomized placebo-controlled study. J Clin Endocrinol Metab 96, 355–364.10.1210/jc.2010-0636Google Scholar
Weile, V., Josephsen, K. & Fejerskov, O. (1990). Effects of single doses of 1-hydroxyethylidene-1,1-bisphosphonate on the mineralizing front of rat incisor enamel: A microradiographic and scanning electron microscopic study. Arch Oral Biol 35, 857–867.10.1016/0003-9969(90)90064-HGoogle Scholar
Weile, V., Josephsen, K. & Fejerskov, O. (1993). Scanning electron microscopy of final enamel formation in rat mandibular incisors following single injections of 1-hydroxyethylidene-1,1-bisphosphonate. Calcif Tissue Int 52, 318–324.10.1007/BF00296658Google Scholar
Yamada, Y., Fuangtharnthip, P., Tamura, Y., Takagi, Y. & Ohya, K. (2000). Gene expression and immunolocalization of amelogenin in enamel hypoplasia induced by successive injections of bisphosphonate in rat incisors. Arch Oral Biol 45, 207–215.10.1016/S0003-9969(99)00134-XGoogle Scholar