Osteoporosis and periodontal diseases with HIV infection (review)

Relevance. The life expectancy of people with HIV has increased thanks to the use of specific antiretroviral therapy (ART). Currently, one of the urgent medical problems for this cohort is osteoporosis. Immune reconstitution during ART leads to a sustained inflammatory reaction in the body, the release of cytokines, and activation of osteoclasts. Osteoporosis often causes complications in periodontology and implantology. The significant need of HIV-infected people for these types of dental care and the prevalence of periodontitis, including generalized forms, also determine the importance of this issue.

Purpose. To identify the common links in the pathogenesis of systemic (osteoporosis – hereinafter referred to as OP) and local (jaw bones in periodontitis) osteoresorption, the main methods for the diagnosis, treatment and prevention of OP associated with HIV infection, its effect on the results of implantological treatment of adentia in this population.

Materials and methods. Analysis of publications in scientific periodicals on OP + Periodontal Pathology + HIV/AIDS over the past decade (PubMed, Medline, Elibrary).

Results. The etiology of bone structure disorders is multifactorial: chronic inflammation, direct impact of HIV on osteocytes, effect of ART (viral protease inhibitors) on bone metabolism and remodeling. The planning of specific therapeutic interventions should be individualized and aimed at the key links in the pathogenesis of osteoresorption (osteoprotectors, antiinflammatory agents, bisphosphonates, calcium supplements, vitamin D).

Conclusion. The effectiveness of the bisphosphonate therapy of OP in this cohort and DEXA screening to control the risk of osteoresorption suggest a very likely clinically justified implantation method for the treatment of tooth loss in HIV infection. Topical issues of OP and periodontal pathology in connection with the aging of HIV patients should be considered as related. For them, the planning of specific diagnostic (DEXA, biochemical screening) and therapeutic (remineralizing agents, osteoprotectors, etc.) strategies involving narrowly specialized doctors (endocrinologists, gastroenterologists, etc.) becomes a decisive.

1. V. V. Rassokhin, A. A Sizov. Disorders of bone metabolisms in HIV patients: causes and approaches to correction. HIV Infection and Immunosuppressive Disorders. 2014;6(4):82-87. (In Russ.). https://doi.org/10.22328/2077-9828-2014-6-4-82-8

2. M. V. Kozlova, A. M. Mkrtumyan, A. M. Panin. Dental implantation in patients with endocrine pathology (features of bone remodeling, diagnosis and correction of metabolic disorders). Moscow. 2015:200. (In Russ.). https://elibrary.ru/item.asp?id=37422273.

3. A. Sharma, P. L. Flom, J. Weedon, R. S. Klein. Prospective study of bone mineral density changes in aging men with or at risk for HIV infection. AIDS. 2010 Sep 24;24(15):2337-2345. https://doi:10.1097/QAD.0b013e32833d7da7.

4. S. Coaccioli, R. Del Giorno, G. Crapa, C. Sabatini, A. Panaccione, L. Di Cato, A. Lavagna, G. Fatati, A. Paladini, R. Frongillo, A. Puxeddu. Study of bone metabolism in patients with chronic HIV infection. Clin. Ter. 2009:160(6):451-456. https://www.ncbi.nlm.nih.gov/pubmed/20198286.

5. T. T. Brown, R. B. Qaqish. Antiretroviral therapy and the prevalence of osteopenia and osteoporosis: a meta-analytic review. AIDS. 2006;20:2165-2174. https://doi.org/10.1097/qad.0b013e32801022eb.

6. V. A. Triant, T. T. Brown, H. Lee, S. K. Grinspoon. Fracture prevalence among human immunodeficiency virus (HIV)-infected versus non-HIV-infected patients in a large U.S. healthcare system. J. Clin. Endocrinol. Metab. 2008;93:3499-3504. https://doi.org/10.1210/jc.2008-0828.

7. R. Guerri-Fernandez, P. Vestergaard, C. Carbonell, H. Knobel, F. F. Aviles, A. S. Castro, X. Nogues, D. Prieto-Alhambra, A. Diez-Perez. HIV infection is strongly associated with hip fracture risk, independently of age, gender, and comorbidities: a population-based cohort study. J. Bone Miner. Res. 2013;28:1259-1263. https://doi.org/10.1002/jbmr.1874.

8. D. Prieto-Alhambra, R. Guerri-Fernandez, F. De Vries, A. Lalmohamed, M. Bazelier, J. Starup-Linde, A. Diez-Perez, C. Cooper, P. Vestergaard. HIV Infection and Its Association with an Excess Risk of Clinical Fractures: A Nationwide Case-Control Study. AIDS. 2014;66:90-95. https://doi.org/10.1097/qai.0000000000000112.

9. A. Sharma, Q. Shi, D. R. Hoover, K. Anastos, P. C. Tien, M. A. Young, M. H. Cohen, E. T. Golub, D. Gustafson, M. T. Yin. Increased Fracture Incidence in Middle-Aged HIV-Infected and HIV-Uninfected Women: Updated Results from the Women’s Interagency HIV Study. AIDS. 2015;70:54-61. https://doi.org/10.1097/qai.0000000000000674.

10. E. Seminari, A. Castagna, A. Soldarini, L. Galli, G. Fusetti, F. Dorigatti, H. Hasson, A. Danise, M. Guffanti, A. Lazzarin, A. Rubinacci. Osteoprotegerin and bone turnover markers in heavily pretreated HIV-infected patients. HIV Med. 2005;May;6(3):145-150. https://doi.org/10.1111/j.1468-1293.2005.00278.x.

11. M. Bongiovanni, C. Tincati. Bone diseases associated with human immunodeficiency virus infection: pathogenesis, risk factors and clinical management. Curr. Mol. Med. 2006;Jun;№6(4).395-400. http://www.eu-rekaselect.com/56169/article.

12. P. M. Grant, D. Kitch, G. A. McComsey, M. P. Dube, R. Haubrich, J. Huang, S. Riddler, P. Tebas, A. R. Zolopa, A. C. Collier, T. T. Brown. Low Baseline CD4+ Count Is Associated with Greater Bone Mineral Density Loss After Antiretroviral Therapy Initiation. Clin. Infect. Dis. 2013;57:1483-1488. https://doi.org/10.1093/cid/cit538.

13. I. Ofotokun, K. Titanji, A. Vunnava, S. Roser-Page, T. Vikulina, F. Villinger, K. Rogers, A. N. Sheth, C. D. Lahiri, J. L. Lennox, M. N. Weitzmann. Antiretroviral therapy induces a rapid increase in bone resorption that is positively associated with the magnitude of immune reconstitution in HIV infection. AIDS. 2016;30:405-414. https://doi.org/10.1097/qad.0000000000000918.

14. K. Titanji, A. Vunnava, A. N. Sheth, C. Delille, J. L. Lennox, S. E. Sanford, A. Foster, A. Knezevic, K. A. Easley, M. N. Weitzmann, I. Ofotokun. Dysregulated B cell expression of RANKL and OPG correlates with loss of bone mineral density in HIV infection. PLoS Pathog. 2014;Nov;13;10(10):e1004497. https://doi:10.1371/journal.ppat.1004497.

15. M. Neale Weitzmann. Bone and the Immune System. Toxicol Pathol. 2017;Oct;45(7):911-924. https://doi:10.1177/0192623317735316.

16. A. Temmerman, L. Rasmusson, A. Kübler, A. Thor, J. Merheb, M. A. Quirynen. Prospective, Controlled, Multicenter Study to Evaluate the Clinical Outcome of Implant Treatment in Women with Osteoporosis/Osteopenia: 5-Year Results. J Dent Res. 2019 Jan;98(1):84-90. https://doi:10.1177/0022034518798804.

17. G. Giro, L. Chambrone, A. Goldstein, J. A. Rodrigues, E. Zenóbio, M. Feres, L. C. Figueiredo, A. Cassoni, J. A. Shibli. Impact of osteoporosis in dental implants: A systematic review. World J Orthop. 2015;6(2):311-315. https://doi.org/10.5312/wjo.v6.i2.311.

18. P. S. Oliveira, J. A. Rodrigues, J. A. Shibli, A. Piattelli, G. Iezzi, V. Perrotti. Influence of osteoporosis on the osteocyte density of human mandibular bone samples: a controlled histological human study. Clin Oral Implants Res. 2016;Mar;27(3):325-328. https://doi:10.1111/clr.12538.

19. M. Schimmel, M. Srinivasan, G. McKenna, F. Müller. Effect of advanced age and/or systemic medical conditions on dental implant survival: A systematic review and meta-analysis. Clin Oral Implants Res. 2018;Oct;29;Suppl16:311-330. https://doi:10.1111/clr.13288.

20. M. Kozlova, A. Mkrtumiyan, L. Dzikovitskaya, A. Beliakova. Features of dental implantation in men with osteoporosis. Dental Forum. 2016;2:28-32. (In Russ.). https://www.elibrary.ru/item.asp?id=26128219.

21. J. Ata-Ali, F. Ata-Ali, N. Di-Benedetto, L. Bagán, J. V. Bagán. Does HIV infection have an impact upon dental implant osseointegration? A systematic review. Med Oral Pathol Oral Cir Buccal. 2015;May;1;20(3):e347-56. http://dx.doi.org/doi:10.4317/medoral.20408.

22. M. C. May, P. N. Andrews, S. Daher, U. N. Reebye. Prospective cohort study of dental implant success rate in patients with AIDS. Int J Implant Dentistry. 2016;2:20. https://doi.org/10.1186/s40729-016-0053-3.

23. A. Sabbah, J. Hicks, B. MacNeill, A. Arbona, A. Aguilera, Q. Liu, J. Gelfond, W. Gardner. A retrospective analysis of dental implant survival in HIV patients. J Clin Periodontol. 2019;Mar;46(3):363-372. https://doi:10.1111/jcpe.13077.

24. V. V. Povoroznuk, I. P. Maazur. Osteoporosis and periodontal diseases. Periodontology. 2005;3(36):14-19. (In Russ.). https://elibrary.ru/item.asp?id=9483516.

25. A. I. Grudyanov, O. S. Titiova. Dynamics of mineral and calcium metabolism at postmenopausal patients by control mineral metabolism medicaments inclusion, in treatment of chronic generalized periodontitis Periodontology. 2010;3(56):9-13. (In Russ.). https://elibrary.ru/item.asp?id=17069600.

26. R. Guiglia, O. Di Fede, L. Lo Russo, D. Sprini, G. B. Rini, G. Campisi. Osteoporosis, jawbones and periodontal disease. Med Oral Patol Oral Cir Bucal. 2013;Jan;1;18(1):e93-9. http://dx.doi.org/doi:10.4317/medoral.18298.

27. A. Mitronin, D. Avakova. Dental status of patients with osteoporosis end rheumatoid arthritis. Stomotology. 2016;6-2(95):15. (In Russ.). https://www.elibrary.ru/item.asp?id=28362595.

28. L. Chambrone Current status of the influence of osteoporosis on periodontology and implant dentistry. Curr Opin Endocrinol Diabetes Obes. 2016;Dec;23(6):435-439. https://doi:10.1097/med.0000000000000272.

29. L. Feller, N. H. Wood, E. J. Raubenheimer, R. Meyerov, J. Lemmer. Alveolar bone necrosis and spontaneous tooth exfoliation in an HIV-seropositive subject with herpes zoster. SADJ. 2008 Mar;63(2):106-110. https://www.ncbi.nlm.nih.gov/pubmed/18561810.

30. N. Cloarec, O. Zaegel-Faucher, S. Bregigeon, C. E. Cano, C. Chossegros, B. Wajszczak, I. Poizot-Martin. Mandibular osteonecrosis and dental exfoliation after trigeminal zoster in an HIV-infected patient: case report and review of the literature. AIDS. 2014;Jan 28;28(3):448-450. https://doi:10.1097/QAD.0000000000000122.

31. F. Maffezzoni, T. Porcelli, I. Karamouzis, E. Quiros-Roldan, F. Castelli, G. Mazziotti, A. Giustina.. Osteoporosis in Human Immunodeficiency Virus Patients – An Emerging Clinical Concern. Eur Endocrinol. 2014;Feb;10(1):79-83. https://doi.org/10.17925/use.2014.10.01.84.

32. C. Camil, S. Rodionova. Current issues of the diagnosis and treatment of osteoporosis. RMJ. 2016;2(24):65-70. (In Russ.). https://www.elibrary.ru/item.asp?id=26153549.

33. C. M. Holahan, S. Koka, K. A. Kennel, A. L. Weaver, D. A. Assad, F. J. Regennitter, D. Kademani. Effect of osteoporotic status on the survival of titanium dental implants. Int J Oral Maxillofac Implants. 2008;Sep-Oct;23(5):905-910. https://jomi.quintessenz.de/index.php?doc=abstract&abstractID=14653.

34. A. Ghanem, S. V. Kellesarian, T. Abduljabbar, N. Al-Hamoudi, F. Vohra, F. Javed. Role of Osteogenic Coatings on Implant Surfaces in Promoting Bone-To-Implant Contact in Experimental Osteoporosis: A Systematic Review and Meta-Analysis. Implant Dent. 2017;Oct;26(5):770-777. https://doi:10.1097/ID.0000000000000634.

35. X. Dereka, E. Calciolari, N. Donos, N. Mardas. Osseointegration in osteoporotic-like condition: A systematic review of preclinical studies. J Periodontal Res. 2018;Dec;53(6):933-940. https://doi:10.1111/jre.12566.

36. A. I. Shatokhin. HIV-periodontopathys is immunosupression predictor (review). Periodontology. 2012;3(64):3-6. (In Russ.). https://elibrary.ru/item.asp?id=18258258.