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Pamidronate Therapy Increases Trabecular Bone Complexity of Mandibular Condyles in Individuals with Osteogenesis Imperfecta

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Abstract

Patients with Osteogenesis Imperfecta (OI) present extra-skeletal manifestations, including important orodental and craniofacial features as dentinogenesis imperfecta, dental agenesis, failure of maxilla growth and hypotonia of masticatory muscles. These features may compromise vital functions speech and mastication. Studies have demonstrated that cyclic pamidronate infusion, the standard therapy for patients with moderate to severe OI, influences the histomorphometric pattern of different body bones. The present study aimed to investigate the condyle trabecular bone pattern in OI patients. We used fractal dimension (FD) analysis on dental panoramic radiographic images to characterize the mandibular condyle trabecular bone in adolescents diagnosed with OI and treated with pamidronate. Imaging exam of 33 adolescents of both sexes, aged between 12 and 17 years, were analyzed and compared with 99 age- and sex-matched healthy adolescents. FD in patients was significantly lower (1.23 ± 0.15) than in healthy controls (1.29 ± 0.11; p < 0.01). Type of OI, age at treatment onset, and the duration of therapy were variables that showed a statistically significant effect on the FD results. This study demonstrated that the bone architecture of mandibular condyles may be altered in pediatric patients with moderate and severe forms of OI. Also, pamidronate treatment seems to have a positive effect on condyle trabecular bone in these patients. This is supported by our finding that FD values were positively influenced by the length of cyclic pamidronate treatment at the time of imaging, as well as by the age of the individual at treatment onset.

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References

  1. Rauch F, Glorieux FH (2004) Osteogenesis imperfecta. Lancet 24:1377–1385. https://doi.org/10.1016/S0140-6736(04)16051-0

    Article  CAS  Google Scholar 

  2. Trejo P, Rauch F (2016) Osteogenesis imperfecta in children and adolescents—new developments in diagnosis and treatment. Osteoporos Int 27:3427–3437. https://doi.org/10.1007/s00198-016-3723-3

    Article  CAS  PubMed  Google Scholar 

  3. Marini JC, Dang Do AN. Osteogenesis Imperfecta. [Updated 2020 Jul 26]. In: Feingold KR, Anawalt B, Boyce A, et al., editors. Endotext [Internet]. South Dartmouth (MA): MDText.com I. 2000. A from: https://www.ncbi.nlm.nih.gov/books/NBK279109. (2020) Osteogenesis Imperfecta. MDText.com

  4. Marini JC, Forlino A, Bächinger HP et al (2017) Osteogenesis imperfecta. Nat Rev Dis Prim. https://doi.org/10.1038/nrdp.2017.52

    Article  PubMed  Google Scholar 

  5. Forlino A, Marini JC (2016) Osteogenesis imperfecta. Lancet 387:1657–1671. https://doi.org/10.1016/S0140-6736(15)00728-X

    Article  CAS  PubMed  Google Scholar 

  6. Sillence DO, Rimoin DL (1978) Classification of osteogenesis imperfecta. Lancet 311:1041–1042. https://doi.org/10.1016/S0140-6736(78)90763-8

    Article  Google Scholar 

  7. Bonafe L, Cormier-Daire V, Hall C et al (2015) Nosology and classification of genetic skeletal disorders: 2015 revision. Am J Med Genet Part A 167:2869–2892. https://doi.org/10.1002/ajmg.a.37365

    Article  CAS  Google Scholar 

  8. Mortier GR, Cohn DH, Cormier-Daire V et al (2019) Nosology and classification of genetic skeletal disorders: 2019 revision. Am J Med Genet Part A 179:2393–2419. https://doi.org/10.1002/ajmg.a.61366

    Article  PubMed  Google Scholar 

  9. Van Dijk FS, Sillence DO (2014) Osteogenesis imperfecta: clinical diagnosis, nomenclature and severity assessment. Am J Med Genet Part A 164:1470–1481. https://doi.org/10.1002/ajmg.a.36545

    Article  Google Scholar 

  10. Schwartz S, Tsipouras P (1984) Oral findings in osteogenesis imperfecta. Oral Surg Oral Med Oral Pathol 57:161–167. https://doi.org/10.1016/0030-4220(84)90206-8

    Article  CAS  PubMed  Google Scholar 

  11. Waltimo J (1994) Hyperfibers and vesicles in dentin matrix in dentinogenesis imperfecta (Dl) associated with osteogenesis imperfecta (01). J Oral Pathol Med 23:389–389. https://doi.org/10.1111/j.1600-0714.1994.tb00082.x

    Article  CAS  PubMed  Google Scholar 

  12. Foster BL, Ramnitz MS, Gafni RI et al (2014) Rare bone diseases and their dental, oral, and craniofacial manifestations. J Dent Res 93:7S-19S. https://doi.org/10.1177/0022034514529150

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Malmgren B, Tsilingaridis G, Monsef-Johansson N et al (2020) Bisphosphonate therapy and tooth development in children and adolescents with osteogenesis imperfecta. Calcif Tissue Int 107:143–150. https://doi.org/10.1007/s00223-020-00707-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  14. Chetty M, Roberts TS, Stephen L, Beighton P (2017) Craniofacial manifestations in osteogenesis imperfecta type III in South Africa. BDJ Open 3:1–5. https://doi.org/10.1038/bdjopen.2017.21

    Article  Google Scholar 

  15. Bendixen KH, Gjørup H, Baad-Hansen L et al (2018) Temporomandibular disorders and psychosocial status in osteogenesis imperfect—a cross-sectional study. BMC Oral Health 18:6–13. https://doi.org/10.1186/s12903-018-0497-3

    Article  Google Scholar 

  16. Ortega ADOL, Rosa VLM, Figueiredo Zwir LML et al (2007) Anatomic and dynamic aspects of stomatognathic structures in osteogenesis imperfecta: a case report. Cranio J Craniomandib Pract 25:144–149. https://doi.org/10.1179/crn.2007.022

    Article  Google Scholar 

  17. Rauch F, Travers R, Parfitt AM, Glorieux FH (2000) Static and dynamic bone histomorphometry in children with osteogenesis imperfecta. Bone 26:581–589. https://doi.org/10.1016/S8756-3282(00)00269-6

    Article  CAS  PubMed  Google Scholar 

  18. Rauch F, Travers R, Plotkin H, Glorieux FH (2002) The effects of intravenous pamidronate on the bone tissue of children and adolescents with osteogenesis imperfecta. J Clin Invest 110:1293–1299. https://doi.org/10.1172/JCI0215952

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Land C, Rauch F, Travers R, Glorieux FH (2007) Osteogenesis imperfecta type VI in childhood and adolescence: effects of cyclical intravenous pamidronate treatment. Bone 40:638–644. https://doi.org/10.1016/j.bone.2006.10.010

    Article  CAS  PubMed  Google Scholar 

  20. Palomo T, Fassier F, Ouellet J et al (2015) Intravenous bisphosphonate therapy of young children with osteogenesis imperfecta: skeletal findings during follow up throughout the growing years. J Bone Miner Res 30:2150–2157. https://doi.org/10.1002/jbmr.2567

    Article  CAS  PubMed  Google Scholar 

  21. Pinheiro B, Zambrano MB, Vanz AP et al (2019) Cyclic pamidronate treatment for osteogenesis imperfecta: report from a brazilian reference center. Genet Mol Biol 42:252–260. https://doi.org/10.1590/1678-4685-gmb-2018-0097

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  22. Apolinário AC, Figueiredo PT, Guimarães AT et al (2015) Pamidronate affects the mandibular cortex of children with osteogenesis imperfecta. J Dent Res 94:95S-102S. https://doi.org/10.1177/0022034514567334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Apolinario AC, Sindeaux R, De Souza Figueiredo PT et al (2016) Dental panoramic indices and fractal dimension measurements in osteogenesis imperfecta children under pamidronate treatment. Dentomaxillofacial Radiol 45:1–9. https://doi.org/10.1259/dmfr.20150400

    Article  Google Scholar 

  24. Marçal FF, Ribeiro EM, Costa FWG et al (2019) Dental alterations on panoramic radiographs of patients with osteogenesis imperfecta in relation to clinical diagnosis, severity, and bisphosphonate regimen aspects: a STROBE-compliant case-control study. Oral Surg Oral Med Oral Pathol Oral Radiol 128:621–630. https://doi.org/10.1016/j.oooo.2019.07.001

    Article  PubMed  Google Scholar 

  25. Marginean O, Tamasanu C, Mang N et al (2017) Therapy with pamidronate in children with osteogenesis imperfecta. Drug Des Dev Ther 11:2507

    Article  CAS  Google Scholar 

  26. Pachêco-Pereira C, Almeida FT, Chavda S et al (2019) Dental imaging of trabecular bone structure for systemic disorder screening: a systematic review. Oral Dis 25:1009–1026. https://doi.org/10.1111/odi.12950

    Article  PubMed  Google Scholar 

  27. Aktuna Belgin C, Serindere G (2020) Fractal and radiomorphometric analysis of mandibular bone changes in patients undergoing intravenous corticosteroid therapy. Oral Surg Oral Med Oral Pathol Oral Radiol 130:110–115. https://doi.org/10.1016/j.oooo.2019.12.009

    Article  PubMed  Google Scholar 

  28. Şahin O, Odabaşı O, Demiralp KÖ et al (2019) Comparison of findings of radiographic and fractal dimension analyses on panoramic radiographs of patients with early-stage and advanced-stage medication-related osteonecrosis of the jaw. Oral Surg Oral Med Oral Pathol Oral Radiol 128:78–86. https://doi.org/10.1016/j.oooo.2019.03.002

    Article  PubMed  Google Scholar 

  29. Neves FS, Barros AS, Cerqueira GA et al (2020) Assessment of fractal dimension and panoramic radiomorphometric indices in women with celiac disease. Oral Radiol 36:141–147. https://doi.org/10.1007/s11282-019-00388-z

    Article  PubMed  Google Scholar 

  30. Baksi BG, Fidler A (2011) Fractal analysis of periapical bone from lossy compressed radiographs: a comparison of two lossy compression methods. J Digit Imaging 24:993–998. https://doi.org/10.1007/s10278-011-9383-0

    Article  PubMed  PubMed Central  Google Scholar 

  31. Toghyani S, Nasseh I, Aoun G, Noujeim M (2019) Effect of image resolution and compression on fractal analysis of the periapical bone. Acta Inform Medica 27:167–170. https://doi.org/10.5455/aim.2019.27.167-170

    Article  Google Scholar 

  32. Bollen AM, Taguchi A, Hujoel PP, Hollender LG (2001) Fractal dimension on dental radiographs. Dentomaxillofacial Radiol 30:270–275. https://doi.org/10.1038/sj.dmfr.4600630

    Article  CAS  Google Scholar 

  33. Law AN, Bollen AM, Chen SK (1996) Detecting osteoporosis using dental radiographs: a comparison of four methods. J Am Dent Assoc 127:1734–1742. https://doi.org/10.14219/jada.archive.1996.0134

    Article  CAS  PubMed  Google Scholar 

  34. Arsan B, Köse TE, Çene E, Özcan İ (2017) Assessment of the trabecular structure of mandibular condyles in patients with temporomandibular disorders using fractal analysis. Oral Surg Oral Med Oral Pathol Oral Radiol 123:382–391. https://doi.org/10.1016/j.oooo.2016.11.005

    Article  PubMed  Google Scholar 

  35. Rasband WS (2018) ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA. https://imagej.nih.gov/ij/.

  36. Sindeaux R, Figueiredo PTDS, De Melo NS et al (2014) Fractal dimension and mandibular cortical width in normal and osteoporotic men and women. Maturitas 77:142–148. https://doi.org/10.1016/j.maturitas.2013.10.011

    Article  PubMed  Google Scholar 

  37. White SC, Rudolph DJ (1999) Alterations of the trabecular pattern of the jaws in patients with osteoporosis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod 88:628–635. https://doi.org/10.1016/S1079-2104(99)70097-1

    Article  CAS  PubMed  Google Scholar 

  38. Smartt JM, Low DW, Bartlett SP (2005) The pediatric mandible: I. A primer on growth and development. Plast Reconstr Surg 116:258. https://doi.org/10.1097/01.prs.0000169940.69315.9c

    Article  CAS  Google Scholar 

  39. Karlo CA, Stolzmann P, Habernig S et al (2010) Size, shape and age-related changes of the mandibular condyle during childhood. Eur Radiol 20:2512–2517. https://doi.org/10.1007/s00330-010-1828-1

    Article  PubMed  Google Scholar 

  40. Bender ME, Lipin RB, Goudy SL (2018) Development of the pediatric temporomandibular joint. Oral Maxillofac Surg Clin North Am 30:1–9. https://doi.org/10.1016/j.coms.2017.09.002

    Article  PubMed  Google Scholar 

  41. Malmgren B, Thesleff I, Dahllöf G et al (2021) Abnormalities in tooth formation after early bisphosphonate treatment in children with osteogenesis imperfecta. Calcif Tissue Int. https://doi.org/10.1007/s00223-021-00835-2

    Article  PubMed  PubMed Central  Google Scholar 

  42. Oliveira ML, Pedrosa EFNC, Cruz AD et al (2013) Relationship between bone mineral density and trabecular bone pattern in postmenopausal osteoporotic Brazilian women. Clin Oral Investig 17:1847–1853. https://doi.org/10.1007/s00784-012-0882-2

    Article  PubMed  Google Scholar 

  43. Parfitt AM, Travers R, Rauch F, Glorieux FH (2000) Structural and cellular changes during bone growth in healthy children. Bone 27:487–494. https://doi.org/10.1016/S8756-3282(00)00353-7

    Article  CAS  PubMed  Google Scholar 

  44. Hegde S, Praveen B, Shetty SR (2013) Morphological and radiological variations of mandibular condyles in health and diseases: a systematic review. Dentistry 03:1–5. https://doi.org/10.4172/2161-1122.1000154

    Article  Google Scholar 

  45. Dwan K, Ca P, Rd S, Basel D (2016) Bisphosphonate therapy for osteogenesis imperfecta (review). Cochrane Libr. https://doi.org/10.1002/14651858.CD005088.pub4

    Article  Google Scholar 

  46. Chagas CEA, Roque JP, Santarosa Emo Peters B et al (2012) Do patients with osteogenesis imperfecta need individualized nutritional support? Nutrition 28:138–142. https://doi.org/10.1016/j.nut.2011.04.003

    Article  PubMed  Google Scholar 

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Funding

The author Pantoja, LLQ was supported by Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES), Ministry of Education, Brazil. This study was supported by a CAPES/COFECUB grant (#918/2018). The authors thank the Department of Research and Innovation, University of Brasilia, Brazil. The funding agencies have no role in the submitted work.

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Authors and Affiliations

  1. Oral Care Center for Inherited Diseases, University of Brasília, Brasília, DF, Brazil

    Letícia L. Quirino Pantoja, Mariana Lustosa, Paulo Márcio Yamaguti, André Ferreira Leite, Paulo Tadeu S. Figueiredo & Ana Carolina Acevedo

  2. Laboratory of Oral Histopathology, Faculty of Healthy Science, University of Brasília, Brasília, DF, Brazil

    Lídia S. Rosa & Ana Carolina Acevedo

  3. Department of Radiology, Faculty of Healthy Science, University of Brasília, Brasília, DF, Brazil

    André Ferreira Leite & Paulo Tadeu S. Figueiredo

  4. Pediatric Endocrinology Department, University Hospital of University of Brasília, Brasília, DF, Brazil

    Luiz Claudio Castro

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  1. Letícia L. Quirino Pantoja
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  2. Mariana Lustosa
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  3. Paulo Márcio Yamaguti
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  8. Ana Carolina Acevedo
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Contributions

LLQP: Contributed to conception, design, data acquisition and interpretation, performed statistical analyses, drafted and critically revised the manuscript. ML: Contributed to data acquisition and interpretation, performed statistical analyses, drafted, and critically revised the manuscript. PMY: Contributed to design, and critically revised the manuscript. LSR: Contributed to design, and critically revised the manuscript. AFL: Contributed to conception, design, data interpretation, revised statistical analyses, and critically revised the manuscript. PTSF: Contributed to design, data interpretation, and critically revised the manuscript. LCC: Contributed to conception, design, data analysis and interpretation, and critically revised the manuscript. ACA: Contributed to conception, design, data analysis and interpretation, drafted and critically revised the manuscript. All authors gave their final approval and agreed to be accountable for all aspects of the work.

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Correspondence to Ana Carolina Acevedo.

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Conflict of Interest

Leticia L. Quirino Pantoja, Mariana Lustosa, Paulo Márcio Yamaguti, Lídia S. Rosa, André Ferreira Leite, Paulo Tadeu S. Figueiredo, Luiz Claudio Castro and Ana Carolina Acevedo declare no potential conflicts of interest with respect to the authorship and/or publication of this article.

Human and Animal Rights and Informed Consent statements

This study was developed at the University Hospital of Brasília (HUB) and approved by the Human Research Ethics Committee of the University of Brasília School of Health Sciences (registration number 15367519.8.0000.0030). Parents or legal guardians of all subjects participating in the study signed an Informed Consent Form, in which they agreed to participate in the research. Parents or legal guardians of all subjects participating in the study signed an Informed Consent Form, in which they allowed publication of data and images.

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Pantoja, L.L.Q., Lustosa, M., Yamaguti, P.M. et al. Pamidronate Therapy Increases Trabecular Bone Complexity of Mandibular Condyles in Individuals with Osteogenesis Imperfecta. Calcif Tissue Int 110, 303–312 (2022). https://doi.org/10.1007/s00223-021-00915-3

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