Sexual dimorphism in the assessment of mineral apposition rate during osteoporosis

Authors

DOI:

https://doi.org/10.33448/rsd-v10i2.12200

Keywords:

Osteoporosis; Sex characteristics; Microscopy.

Abstract

The objective of this study was to evaluate the daily maxillary and tibial bone mineral apposition rate of ovariectomized rats and orchiectomized rats through confocal laser microscopy. Twenty-four animals were divided into 4 groups (SHAMF, OVX, SHAMM and ORQ). Six rats were distributed to the SHAMF group (submitted to fictitious surgery); six rats to the OVX group (submitted to bilateral ovariectomy); six rats to the SHAMM group (submitted to fictitious surgery) and six rats to the ORQ group (submitted to bilateral orchiectomy). On the 60th day after the surgical procedures the animals received 20 mg/kg of calcein and after 24 days 20 mg/kg of alizarin red was administered. The euthanasia was performed 18 days after the last fluorochrome administration. The histological slides obtained were submitted to confocal microscopy analysis and then dynamic histomorphometry was performed to obtain the daily mineral apposition rate (MAR). In the tibias, the values of MAR were higher for the SHAMF group (P<0.05) (mean: 37.1μm² / day) compared to the ORQ group (mean: 7.16 μm²). In the jaws, the values were higher for the SHAMF group (P<0.05) (mean: 5.175μm² / day) compared to the SHAMM group (mean: 1.84 μm²), OVX (mean: 3.027 μm²) and ORQ group (mean: 1.56 μm²). It can be concluded that the female gender, regarding the characteristics of the maxillary and tibial bones, presented a daily mineral bone apposition rate higher than the male gender, mainly in the maxillary bone, presenting a statistically significant difference between all groups studied.

References

Akbaba, G., Isik, S., Ates Tutuncu, Y., Ozuguz, U., Berker, D., & Guler, S. (2013). Comparison of alendronate and raloxifene for the management of primary hyperparathyroidism. Journal of endocrinological investigation, 36(11), 1076–1082. https://doi.org/10.3275/9095

Alghamdi, H. S., van den Beucken, J. J., & Jansen, J. A. (2014). Osteoporotic rat models for evaluation of osseointegration of bone implants. Tissue engineering. Part C, Methods, 20(6), 493–505. https://doi.org/10.1089/ten.TEC.2013.0327

Al-Shahat, A. R., Shaikh, M. A., Elmansy, R. A., Shehzad, K., & Kaimkhani, Z. A. (2011). Prostatic assessment in rats after bilateral orchidectomy and calcitonin treatment. Endocrine regulations, 45(1), 29–36.

Annibali, S., Cristalli, M. P., Dell'Aquila, D., Bignozzi, I., La Monaca, G., & Pilloni, A. (2012). Short dental implants: a systematic review. Journal of dental research, 91(1), 25–32. https://doi.org/10.1177/0022034511425675

Aubin, J. E., & Bonnelye, E. (2000). Osteoprotegerin and its ligand: A new paradigm for regulation of osteoclastogenesis and bone resorption. Medscape women's health, 5(2), 5

de Oliveira Puttini, I., Gomes-Ferreira, P., de Oliveira, D., Hassumi, J. S., Gonçalves, P. Z., & Okamoto, R. (2019). Teriparatide improves alveolar bone modelling after tooth extraction in orchiectomized rats. Archives of oral biology, 102, 147–154. https://doi.org/10.1016/j.archoralbio.2019.04.007

Dempster, D. W., Compston, J. E., Drezner, M. K., Glorieux, F. H., Kanis, J. A., Malluche, H., Meunier, P. J., Ott, S. M., Recker, R. R., & Parfitt, A. M. (2013). Standardized nomenclature, symbols, and units for bone histomorphometry: a 2012 update of the report of the ASBMR Histomorphometry Nomenclature Committee. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research, 28(1), 2–17. https://doi.org/10.1002/jbmr.1805

Drage, N. A., Palmer, R. M., Blake, G., Wilson, R., Crane, F., & Fogelman, I. (2007). A comparison of bone mineral density in the spine, hip and jaws of edentulous subjects. Clinical oral implants research, 18(4), 496–500. https://doi.org/10.1111/j.1600-0501.2007.01379.x

Drake, M. T., & Khosla, S. (2012). Male osteoporosis. Endocrinology and metabolism clinics of North America, 41(3), 629–641. https://doi.org/10.1016/j.ecl.2012.05.001

Farahmand, P., Spiegel, R., & Ringe, J. D. (2016). Männliche Osteoporose [Male osteoporosis]. Zeitschrift fur Rheumatologie, 75(5), 459–465. https://doi.org/10.1007/s00393-016-0078-2

Gennari, L., Nuti, R., & Bilezikian, J. P. (2004). Aromatase activity and bone homeostasis in men. The Journal of clinical endocrinology and metabolism, 89(12), 5898–5907. https://doi.org/10.1210/jc.2004-1717

Giusti, A., & Bianchi, G. (2014). Treatment of primary osteoporosis in men. Clinical interventions in aging, 10, 105–115. https://doi.org/10.2147/CIA.S44057

Hassler, N., Roschger, A., Gamsjaeger, S., Kramer, I., Lueger, S., van Lierop, A., Roschger, P., Klaushofer, K., Paschalis, E. P., Kneissel, M., & Papapoulos, S. (2014). Sclerostin deficiency is linked to altered bone composition. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research, 29(10), 2144–2151. https://doi.org/10.1002/jbmr.2259

Häuselmann, H. J., & Rizzoli, R. (2003). A comprehensive review of treatments for postmenopausal osteoporosis. Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA, 14(1), 2–12. https://doi.org/10.1007/s00198-002-1301-3

Kaufman, J. M., & Goemaere, S. (2008). Osteoporosis in men. Best practice & research. Clinical endocrinology & metabolism, 22(5), 787–812. https://doi.org/10.1016/j.beem.2008.09.005

Kaufman, J. M., Lapauw, B., & Goemaere, S. (2014). Current and future treatments of osteoporosis in men. Best practice & research. Clinical endocrinology & metabolism, 28(6), 871–884. https://doi.org/10.1016/j.beem.2014.09.002

Kilkenny, C., Browne, W. J., Cuthi, I., Emerson, M., & Altman, D. G. (2012). Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. Veterinary clinical pathology, 41(1), 27–31. https://doi.org/10.1111/j.1939-165X.2012.00418.x

Luvizuto, E. R., Queiroz, T. P., Dias, S. M., Okamoto, T., Dornelles, R. C., Garcia, I. R., Jr, & Okamoto, R. (2010). Histomorphometric analysis and immunolocalization of RANKL and OPG during the alveolar healing process in female ovariectomized rats treated with oestrogen or raloxifene. Archives of oral biology, 55(1), 52–59. https://doi.org/10.1016/j.archoralbio.2009.11.001

Manolagas, S. C., & Jilka, R. L. (1995). Bone marrow, cytokines, and bone remodeling. Emerging insights into the pathophysiology of osteoporosis. The New England journal of medicine, 332(5), 305–311. https://doi.org/10.1056/NEJM199502023320506

Marie P. J. (2006). Strontium ranelate: a dual mode of action rebalancing bone turnover in favour of bone formation. Current opinion in rheumatology, 18 Suppl 1, S11–S15. https://doi.org/10.1097/01.bor.0000229522.89546.7b

Marie, P. J., Hott, M., Modrowski, D., De Pollak, C., Guillemain, J., Deloffre, P., & Tsouderos, Y. (1993). An uncoupling agent containing strontium prevents bone loss by depressing bone resorption and maintaining bone formation in estrogen-deficient rats. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research, 8(5), 607–615. https://doi.org/10.1002/jbmr.5650080512

Marx, R. E., Cillo, J. E., Jr, & Ulloa, J. J. (2007). Oral bisphosphonate-induced osteonecrosis: risk factors, prediction of risk using serum CTX testing, prevention, and treatment. Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons, 65(12), 2397–2410. https://doi.org/10.1016/j.joms.2007.08.003

McClung, M. R., Lewiecki, E. M., Cohen, S. B., Bolognese, M. A., Woodson, G. C., Moffett, A. H., Peacock, M., Miller, P. D., Lederman, S. N., Chesnut, C. H., Lain, D., Kivitz, A. J., Holloway, D. L., Zhang, C., Peterson, M. C., Bekker, P. J., & AMG 162 Bone Loss Study Group (2006). Denosumab in postmenopausal women with low bone mineral density. The New England journal of medicine, 354(8), 821–831. https://doi.org/10.1056/NEJMoa044459

Mittan, D., Lee, S., Miller, E., Perez, R. C., Basler, J. W., & Bruder, J. M. (2002). Bone loss following hypogonadism in men with prostate cancer treated with GnRH analogs. The Journal of clinical endocrinology and metabolism, 87(8), 3656–3661. https://doi.org/10.1210/jcem.87.8.8782

NIH Consensus Development Panel on Osteoporosis Prevention, Diagnosis, and Therapy (2001). Osteoporosis prevention, diagnosis, and therapy. JAMA, 285(6), 785–795. https://doi.org/10.1001/jama.285.6.785

Oliveira, L. G., & Guimarães, M. L. (2015). MALE OSTEOPOROSIS. Revista brasileira de ortopedia, 45(5), 392–396. https://doi.org/10.1016/S2255-4971(15)30425-0

Pacifici, R., Rifas, L., McCracken, R., Vered, I., McMurtry, C., Avioli, L. V., & Peck, W. A. (1989). Ovarian steroid treatment blocks a postmenopausal increase in blood monocyte interleukin 1 release. Proceedings of the National Academy of Sciences of the United States of America, 86(7), 2398–2402. https://doi.org/10.1073/pnas.86.7.2398

Pedrosa, W. F., Jr, Okamoto, R., Faria, P. E., Arnez, M. F., Xavier, S. P., & Salata, L. A. (2009). Immunohistochemical, tomographic and histological study on onlay bone graft remodeling. Part II: calvarial bone. Clinical oral implants research, 20(11), 1254–1264. https://doi.org/10.1111/j.1600-0501.2009.01747.x

Pereira, A. S; Shitsuka, D. M; Pereira, F. J; Shitsuka, R. (2018). Scientific research methodology. [eBook]. Santa Maria: Ed. UAB / NTE / UFSM. Retrieved from: at: https://repositorio.ufsm.br/bitstream/handle/1/15824/Lic_Computacao_Metodologia-Pesquisa-Cientifica.pdf?sequence=1.

Ramalho-Ferreira, G., Faverani, L. P., Grossi-Oliveira, G. A., Okamoto, T., & Okamoto, R. (2015). Alveolar bone dynamics in osteoporotic rats treated with raloxifene or alendronate: confocal microscopy analysis. Journal of biomedical optics, 20(3), 038003. https://doi.org/10.1117/1.JBO.20.3.038003

Ramalho-Ferreira, G., Faverani, L. P., Momesso, G., Luvizuto, E. R., de Oliveira Puttini, I., & Okamoto, R. (2017). Effect of antiresorptive drugs in the alveolar bone healing. A histometric and immunohistochemical study in ovariectomized rats. Clinical oral investigations, 21(5), 1485–1494. https://doi.org/10.1007/s00784-016-1909-x

Riggs, B. L., Khosla, S., & Melton, L. J., 3rd (2002). Sex steroids and the construction and conservation of the adult skeleton. Endocrine reviews, 23(3), 279–302. https://doi.org/10.1210/edrv.23.3.0465

Ruggiero, S. L., Dodson, T. B., Fantasia, J., Goodday, R., Aghaloo, T., Mehrotra, B., O'Ryan, F., & American Association of Oral and Maxillofacial Surgeons (2014). American Association of Oral and Maxillofacial Surgeons position paper on medication-related osteonecrosis of the jaw--2014 update. Journal of oral and maxillofacial surgery : official journal of the American Association of Oral and Maxillofacial Surgeons, 72(10), 1938–1956. https://doi.org/10.1016/j.joms.2014.04.031

Sayed, A. A., Soliman, A. M., Fahmy, S. R., Marzouk, M. (2013) Antiosteoporotic effect of Coelatura aegyptiaca shell powder on ovariectomized rats. African Journal of Pharmacy and Pharmacology 7(34), 2406-2416. https://doi.org/10.5897/AJPP2013.3817

Seeman E. (2003). Reduced bone formation and increased bone resorption: rational targets for the treatment of osteoporosis. Osteoporosis international : a journal established as result of cooperation between the European Foundation for Osteoporosis and the National Osteoporosis Foundation of the USA, 14 Suppl 3, S2–S8. https://doi.org/10.1007/s00198-002-1340-9

Seifi, M., Ezzati, B., Saedi, S., & Hedayati, M. (2015). The Effect of Ovariectomy and Orchiectomy on Orthodontic Tooth Movement and Root Resorption in Wistar Rats. Journal of dentistry (Shiraz, Iran), 16(4), 302–309.

Stevenson, M., Jones, M. L., De Nigris, E., Brewer, N., Davis, S., & Oakley, J. (2005). A systematic review and economic evaluation of alendronate, etidronate, risedronate, raloxifene and teriparatide for the prevention and treatment of postmenopausal osteoporosis. Health technology assessment (Winchester, England), 9(22), 1–160. https://doi.org/10.3310/hta9220 G.

Vanderschueren, D., Vandenput, L., Boonen, S., Lindberg, M. K., Bouillon, R., & Ohlsson, C. (2004). Androgens and bone. Endocrine reviews, 25(3), 389–425. https://doi.org/10.1210/er.2003-0003

Van Pottelbergh, I., Goemaere, S., & Kaufman, J. M. (2003). Bioavailable estradiol and an aromatase gene polymorphism are determinants of bone mineral density changes in men over 70 years of age. The Journal of clinical endocrinology and metabolism, 88(7), 3075–3081. https://doi.org/10.1210/jc.2002-021691

Wang, N., Docherty, F. E., Brown, H. K., Reeves, K. J., Fowles, A. C., Ottewell, P. D., Dear, T. N., Holen, I., Croucher, P. I., & Eaton, C. L. (2014). Prostate cancer cells preferentially home to osteoblast-rich areas in the early stages of bone metastasis: evidence from in vivo models. Journal of bone and mineral research : the official journal of the American Society for Bone and Mineral Research, 29(12), 2688–2696. https://doi.org/10.1002/jbmr.2300

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03/02/2021

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COLÉTE, . J. Z.; FERREIRA, P. H. S. G. .; FRIGÉRIO, P. B.; PUTTINI, I. de O. .; MOMESSO, G. .; BATISTA, F. R. de S.; OKAMOTO, . R. . Sexual dimorphism in the assessment of mineral apposition rate during osteoporosis. Research, Society and Development, [S. l.], v. 10, n. 2, p. e4910212200, 2021. DOI: 10.33448/rsd-v10i2.12200. Disponível em: https://rsdjournal.org/index.php/rsd/article/view/12200. Acesso em: 16 nov. 2024.

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Vol. 10 No. 2

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Copyright (c) 2021 Juliana Zorzi Coléte; Pedro Henrique Silva Gomes Ferreira; Paula Buzo Frigério; Igor de Oliveira Puttini; Gustavo Momesso; Fábio Roberto de Souza Batista; Roberta Okamoto

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