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CC BY 4.0 · Eur J Dent 2024; 18(04): 997-1003
DOI: 10.1055/s-0044-1785533
Review Article

Influence of Osteoporosis on the Course of Apical Periodontitis

Evgeni Stanev 
1   Department of Conservative Dentistry, Faculty of Dental Medicine, Medical University of Sofia, Sofia, Bulgaria
,
Radosveta Ivanova Vasileva
1   Department of Conservative Dentistry, Faculty of Dental Medicine, Medical University of Sofia, Sofia, Bulgaria
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Abstract

Osteoporosis is a disease characterized by disruption of the bone microarchitecture. It is observed in both sexes, but to a greater extent in women. It affects the whole body, including the jaws. The main indicator of the presence of osteoporosis accepted by the World Health Organization is bone mineral density. The aim of this article is to find data on the influence of osteoporosis on apical periodontitis, to investigate how the intake of osteoporosis drugs affects apical periodontitis, and to establish various data that may be of benefit to the dental practitioner when treating patients with osteoporosis and apical periodontitis. Open-access publications are included. The presence of osteoporosis is important to the dentist. Apical periodontitis in these patients has a faster progression. They are characterized by inflammation and destruction of the tissues located around the tooth root. Osteoporosis has a destructive effect on bone tissue through different mechanisms: nuclear factor-κβ ligand and NLRP3/Caspase-1/IL-1β cascade. It is also associated with low estrogen levels. Various medications such as corticosteroids, bisphosphonates (alendronate, zoledronate (Zoledronic acid), calcitonin, raloxifene, and strontium used to treat osteoporosis can affect the course of apical periodontitis. When treating patients with periapical lesions, the dentist must take a proper medical history and general medical history. In cases of osteoporosis or taking bisphosphonates and other medications, consideration should be given to whether consultation with a specialist is necessary, what treatment approach would be most appropriate, and what the prognosis will be. Chronic diseases affect both the general state of the body and dental health. It has been found that in patients with osteoporosis, inflammation of the apical periodontium develops with faster bone resorption. Before starting dental treatment, it is important to specify the etiology of osteoporosis, the bone density of each patient, as well as the medications they are taking.

Keywords

osteoporosis - apical periodontitis - corticosteroids - bisphosphonates - bone resorption - calcitonin - raloxifene - alendronate - zoledronate


Publication History

Article published online:
17 May 2024

© 2024. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution License, permitting unrestricted use, distribution, and reproduction so long as the original work is properly cited. (https://creativecommons.org/licenses/by/4.0/)

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  • References

  • 1 Sözen T, Özışık L, Başaran NÇ. An overview and management of osteoporosis. Eur J Rheumatol 2017; 4 (01) 46-56
    CrossrefPubMedGoogle Scholar
  • 2 Wright NC, Looker AC, Saag KG. et al. The recent prevalence of osteoporosis and low bone mass in the United States based on bone mineral density at the femoral neck or lumbar spine. J Bone Miner Res 2014; 29 (11) 2520-2526
    CrossrefPubMedGoogle Scholar
  • 3 Tuzun S, Eskiyurt N, Akarirmak U. et al; Turkish Osteoporosis Society. Incidence of hip fracture and prevalence of osteoporosis in Turkey: the FRACTURK study. Osteoporos Int 2012; 23 (03) 949-955
    CrossrefPubMedGoogle Scholar
  • 4 Salari N, Ghasemi H, Mohammadi L, Rabieenia E, Shohaimi S, Mohammadi M. The global prevalence of osteoporosis in the world: a comprehensive systematic review and meta-analysis. J Orthop Surg Res 2021; 16 (01) 1-20
    PubMedGoogle Scholar
  • 5 Kanis JA, McCloskey EV, Johansson H, Cooper C, Rizzoli R, Reginster JY. Scientific Advisory Board of the European Society for Clinical and Economic Aspects of Osteoporosis and Osteoarthritis (ESCEO) and the Committee of Scientific Advisors of the International Osteoporosis Foundation (IOF). European guidance for the diagnosis and management of osteoporosis in postmenopausal women. Osteoporos Int 2013; 24 (01) 23-57
    CrossrefPubMedGoogle Scholar
  • 6 Poole KE, Compston JE. Osteoporosis and its management. BMJ 2006; 333 (7581) 1251-1256
    CrossrefPubMedGoogle Scholar
  • 7 Cosman F, de Beur SJ, LeBoff MS. et al; National Osteoporosis Foundation. Clinician's guide to prevention and treatment of osteoporosis. Osteoporos Int 2014; 25 (10) 2359-2381
    CrossrefPubMedGoogle Scholar
  • 8 Li L, Wang Z. Ovarian aging and osteoporosis. Adv Exp Med Biol 2018; 1086: 199-215
    CrossrefPubMedGoogle Scholar
  • 9 Compston J, Bowring C, Cooper A. et al; National Osteoporosis Guideline Group. Diagnosis and management of osteoporosis in postmenopausal women and older men in the UK: National Osteoporosis Guideline Group (NOGG) update 2013. Maturitas 2013; 75 (04) 392-396
    CrossrefPubMedGoogle Scholar
  • 10 D'Amelio P, Isaia GC. Male Osteoporosis in the Elderly. Int J Endocrinol 2015; 2015: 907689
    PubMedGoogle Scholar
  • 11 Tounta TS. Diagnosis of osteoporosis in dental patients. J Frailty Sarcopenia Falls 2017; 2 (02) 21-27
    CrossrefPubMedGoogle Scholar
  • 12 Astuti ER, Arifin AZ, Indraswari R, Putra RH, Ramadhani NF, Pramatika B. Computer-aided system of the mandibular cortical bone porosity assessment on digital panoramic radiographs. Eur J Dent 2023; 17 (02) 464-471
    Article in Thieme ConnectPubMedGoogle Scholar
  • 13 Ramadan DE, Hariyani N, Indrawati R, Ridwan RD, Diyatri I. Cytokines and chemokines in periodontitis. Eur J Dent 2020; 14 (03) 483-495
    Article in Thieme ConnectPubMedGoogle Scholar
  • 14 Brasil SC, Santos RMM, Fernandes A. et al. Influence of oestrogen deficiency on the development of apical periodontitis. Int Endod J 2017; 50 (02) 161-166
    CrossrefPubMedGoogle Scholar
  • 15 Cheng CH, Chen LR, Chen KH. Osteoporosis due to hormone imbalance: an overview of the effects of estrogen deficiency and glucocorticoid overuse on bone turnover. Int J Mol Sci 2022; 23 (03) 1376
    CrossrefPubMedGoogle Scholar
  • 16 Zhang X, Peng B, Fan M, Bian Z, Chen Z. The effect of estrogen deficiency on receptor activator of nuclear factor kappa B ligand and osteoprotegerin synthesis in periapical lesions induced in rats. J Endod 2007; 33 (09) 1053-1056
    CrossrefPubMedGoogle Scholar
  • 17 Schäfer E. Root canal treatment and general medicine. Zahnmedizin up2date 2023; 17 (01) 21-32
    Google Scholar
  • 18 Özden FO, Sakallioğlu EE, Demir E. et al. Effect of bisphosphonate as an adjunct treatment for chronic periodontitis on gingival crevicular fluid levels of nuclear factor-κB ligand (RANKL) and osteoprotegerin in postmenopausal osteoporosis. J Oral Sci 2017; 59 (01) 147-155
    CrossrefPubMedGoogle Scholar
  • 19 Ikeda M, Karakawa A, Takizawa H. et al. Effects of anti-receptor activator of nuclear factor kappa b ligand antibody and zoledronic acid on periapical lesion development in mice. J Endod 2022; 48 (05) 632-640
    CrossrefPubMedGoogle Scholar
  • 20 Streicher C, Heyny A, Andrukhova O. et al. Estrogen regulates bone turnover by targeting RANKL expression in bone lining cells. Sci Rep 2017; 7 (01) 6460
    CrossrefPubMedGoogle Scholar
  • 21 Castro MML, Ferreira RO, Fagundes NCF, Almeida APCPSC, Maia LC, Lima RR. Association between psychological stress and periodontitis: a systematic review. Eur J Dent 2020; 14 (01) 171-179
    Article in Thieme ConnectPubMedGoogle Scholar
  • 22 Zhen Y, Zhang H. NLRP3 inflammasome and inflammatory bowel disease. Front Immunol 2019; 10: 276
    CrossrefPubMedGoogle Scholar
  • 23 Majeed MM, Ahmed I, Roome T, Fatima T, Amin R. Association between interleukin-1β gene polymorphism and chronic periodontitis. Eur J Dent 2021; 15 (04) 702-706
    Article in Thieme ConnectPubMedGoogle Scholar
  • 24 Grigoriadis A, Räisänen IT, Pärnänen P, Tervahartiala T, Sorsa T, Sakellari D. Is There a link between COVID-19 and periodontal disease? A narrative review. Eur J Dent 2022; 16 (03) 514-520
    Article in Thieme ConnectPubMedGoogle Scholar
  • 25 Luthfi M, Razak FA, Kusumawardhani DP, Nagoro AAB, Fadhila N. The effect of Centella asiatica methanolic extract on expression of IL-1β proinflammatory cytokines in severe early childhood caries. Eur J Dent 2023; 17 (04) 1037-1042
    Article in Thieme ConnectPubMedGoogle Scholar
  • 26 Rajagopal A, Varghese J, Bhat V, Acharya V, Kamath V. Anti-infective efficacy of mechanical debridement with adjunctive modalities on clinical and cytokine parameters in treatment of chronic periodontitis: randomized controlled clinical trial. Eur J Dent 2024; 18 (02) 526-533
    Article in Thieme ConnectPubMedGoogle Scholar
  • 27 Kainat R, Ahmed I, Alolaywi AM, Waheed H, Sultan ZK, Moin SF. Assessment of salivary MMP-8 and IL-1β for the diagnosis of periodontal diseases in Pakistani population. Eur J Dent 2024; 18 (02) 672-679
    Article in Thieme ConnectPubMedGoogle Scholar
  • 28 Liu S, Li Q, Liu Y. Immunohistochemical localization of NALP3 inflammasome in experimental periapical lesions. Int Endod J 2014; 47 (10) 949-957
    CrossrefPubMedGoogle Scholar
  • 29 Ran S, Liu B, Gu S, Sun Z, Liang J. Analysis of the expression of NLRP3 and AIM2 in periapical lesions with apical periodontitis and microbial analysis outside the apical segment of teeth. Arch Oral Biol 2017; 78: 39-47
    CrossrefPubMedGoogle Scholar
  • 30 Liu T, Ma Y, Zhang R. et al. Resveratrol ameliorates estrogen deficiency-induced depression- and anxiety-like behaviors and hippocampal inflammation in mice. Psychopharmacology (Berl) 2019; 236 (04) 1385-1399
    CrossrefPubMedGoogle Scholar
  • 31 Guan X, Guan Y, Shi C. et al. Estrogen deficiency aggravates apical periodontitis by regulating NLRP3/caspase-1/IL-1β axis. Am J Transl Res 2020; 12 (02) 660-671
    PubMedGoogle Scholar
  • 32 Romualdo PC, Lucisano MP, Paula-Silva FWG. et al. Ovariectomy exacerbates apical periodontitis in rats with an increase in expression of proinflammatory cytokines and matrix metalloproteinases. J Endod 2018; 44 (05) 780-785
    CrossrefPubMedGoogle Scholar
  • 33 Bahuguna R, Jain A, Khan SA, Arvind MS. Role of odanacatib in reducing bone loss due to endodontic disease: An overview. J Int Soc Prev Community Dent 2016; 6 (3, Suppl 3): S175-S181
    CrossrefPubMedGoogle Scholar
  • 34 Basso L, Chacun D, Sy K, Grosgogeat B, Gritsch K. Periodontal diseases and COVID-19: a scoping review. Eur J Dent 2021; 15 (04) 768-775
    Article in Thieme ConnectPubMedGoogle Scholar
  • 35 Lucisano MP, da Silva RAB, de Sousa Pereira AP. et al. Alteration of the oral microbiota may be a responsible factor, along with estrogen deficiency, by the development of larger periapical lesions. Clin Oral Investig 2021; 25 (06) 3651-3662
    CrossrefPubMedGoogle Scholar
  • 36 Rossetti BR, Lemos AF, Só BB, Weissheimer T, Martins MD, Só MVR. Effects of estrogen deficiency on the progression of apical periodontitis. A systematic review of preclinical studies. Arch Oral Biol 2022; 142: 105496
    CrossrefPubMedGoogle Scholar
  • 37 Jeffcoat MK, Lewis CE, Reddy MS, Wang CY, Redford M. Post-menopausal bone loss and its relationship to oral bone loss. Periodontol 2000 2000; 23 (01) 94-102
    CrossrefPubMedGoogle Scholar
  • 38 López-López J, Castellanos-Cosano L, Estrugo-Devesa A, Gómez-Vaquero C, Velasco-Ortega E, Segura-Egea JJ. Radiolucent periapical lesions and bone mineral density in post-menopausal women. Gerodontology 2015; 32 (03) 195-201
    CrossrefPubMedGoogle Scholar
  • 39 Duncea I, Almasan O, Buduru S, Condor D, Păcurar M, Tig I. THE prevalence of periodontal disease in postmenopausal women with osteoporosis. Romanian J Oral Rehabil 2022; 14 (01) 125-135
    Google Scholar
  • 40 Hsiao A, Glickman G, He J. A retrospective clinical and radiographic study on healing of periradicular lesions in patients taking oral bisphosphonates. J Endod 2009; 35 (11) 1525-1528
    CrossrefPubMedGoogle Scholar
  • 41 Sampaio FC, Veloso HHP, do Nascimento Barbosa D. Mechanisms of action of bisphosphonates and their influence on treatment prognosis. Rev Fac Odontol P Alegre 2010; 51 (01) 31-38
    Google Scholar
  • 42 Jobke B, Milovanovic P, Amling M, Busse B. Bisphosphonate-osteoclasts: changes in osteoclast morphology and function induced by antiresorptive nitrogen-containing bisphosphonate treatment in osteoporosis patients. Bone 2014; 59: 37-43
    CrossrefPubMedGoogle Scholar
  • 43 Katz J, Rotstein I. Prevalence of periapical lesions in patients with osteoporosis. J Endod 2021; 47 (02) 234-238
    CrossrefPubMedGoogle Scholar
  • 44 Cadoni E, Ideo F, Marongiu G. et al. Periapical status in patients affected by osteoporosis: a retrospective clinical study. Clin Exp Dent Res 2022; 8 (05) 1068-1075
    CrossrefPubMedGoogle Scholar
  • 45 Ivanova VV. Socket preservation – clinical, radiographical and histomorphometric evaluation [Ph.D. dissertation]. Plovdiv, Bulgaria: Medical University Plovdiv; 2020
    Google Scholar
  • 46 Chapanov KI, Deliverska-Aleksandrova EG, Naydenov AV. Total oral rehabilitation with dental implants in an elderly patient with concomitant diseases: a case report. Folia Med (Plovdiv) 2021; 63 (06) 1000-1005
    CrossrefPubMedGoogle Scholar
  • 47 Venkatakrishnan CJ, Bhuminathan S, Chandran CR, Poovannan S. Dental implants in patients with osteoporosis–a review. Biomed Pharmacol J 2017; 10 (03) 1415-1418
    CrossrefGoogle Scholar
  • 48 Yarbasi Ö, Bozdemir E. Evaluation of early-stage osteonecrosis findings and oral health in patients using biphosphonate for osteoporosis [in Turkish]. Adnan Menderes Üniversitesi Sağlık Bilimleri Fakültesi Dergisi 2023; 7 (02) 270-280
    Google Scholar
  • 49 Al-Maweri SA, Alshammari MN, Alharbi AR. et al. Knowledge and opinions of Saudi dentists regarding dental treatment of patients undergoing bisphosphonates. Eur J Dent 2020; 14 (01) 144-151
    Article in Thieme ConnectPubMedGoogle Scholar
  • 50 Xiong H, Peng B, Wei L, Zhang X, Wang L. Effect of an estrogen-deficient state and alendronate therapy on bone loss resulting from experimental periapical lesions in rats. J Endod 2007; 33 (11) 1304-1308
    CrossrefPubMedGoogle Scholar
  • 51 Silva RAB, Sousa-Pereira AP, Lucisano MP. et al. Alendronate inhibits osteocyte apoptosis and inflammation via IL-6, inhibiting bone resorption in periapical lesions of ovariectomized rats. Int Endod J 2020; 53 (01) 84-96
    CrossrefPubMedGoogle Scholar
  • 52 Lilakhunakon C, Suwanpateeb J, Patntirapong S. Inhibitory effects of alendronate on adhesion and viability of preosteoblast cells on titanium discs. Eur J Dent 2021; 15 (03) 502-508
    Article in Thieme ConnectPubMedGoogle Scholar
  • 53 Wayama MT, Yoshimura H, Ohba S. et al. Diminished progression of periapical lesions with zoledronic acid in ovariectomized rats. J Endod 2015; 41 (12) 2002-2007
    CrossrefPubMedGoogle Scholar
  • 54 Maia CA, Chaves HGDS, Benetti F. et al. Zoledronic acid modulates cytokine expression and mitigates bone loss during the development of induced apical periodontitis in a mice model. J Endod 2023;S0099-2399(23)00505-8
    Google Scholar
  • 55 Marques-Ferreira M, Abrantes AM, Paula A. et al. The role of apical periodontitis disease in the development of bisphosphonate-related osteonecrosis of the jaw: an animal study. Dent J 2023; 11 (07) 168
    CrossrefPubMedGoogle Scholar
  • 56 Woolf AD. An update on glucocorticoid-induced osteoporosis. Curr Opin Rheumatol 2007; 19 (04) 370-375
    PubMedGoogle Scholar
  • 57 Gomes-Filho JE, Wayama MT, Dornelles RCM. et al. Raloxifene modulates regulators of osteoclastogenesis and angiogenesis in an oestrogen deficiency periapical lesion model. Int Endod J 2015; 48 (11) 1059-1068
    CrossrefPubMedGoogle Scholar
  • 58 Liu S, Cheng Y, Xu W, Bian Z. Protective effects of follicle-stimulating hormone inhibitor on alveolar bone loss resulting from experimental periapical lesions in ovariectomized rats. J Endod 2010; 36 (04) 658-663
    CrossrefPubMedGoogle Scholar
  • 59 Qian H, Jia J, Yang Y, Bian Z, Ji Y. A follicle-stimulating hormone exacerbates the progression of periapical inflammation through modulating the cytokine release in periodontal tissue. Inflammation 2020; 43 (04) 1572-1585
    CrossrefPubMedGoogle Scholar
  • 60 Marie PJ. Strontium as therapy for osteoporosis. Curr Opin Pharmacol 2005; 5 (06) 633-636
    CrossrefPubMedGoogle Scholar
  • 61 Oztekin F, Gurgenc T, Dundar S. et al. In vivo evaluation of the effects of b-doped strontium apatite nanoparticles produced by hydrothermal method on bone repair. J Funct Biomater 2022; 13 (03) 110
    CrossrefPubMedGoogle Scholar
  • 62 Zaheer S, LeBoff M, Lewiecki EM. Denosumab for the treatment of osteoporosis. Expert Opin Drug Metab Toxicol 2015; 11 (03) 461-470
    CrossrefPubMedGoogle Scholar
  • 63 Hasegawa T, Ueda N, Yamada SI. et al; Japanese Study Group of Co-operative Dentistry with Medicine (JCDM). Denosumab-related osteonecrosis of the jaw after tooth extraction and the effects of a short drug holiday in cancer patients: a multicenter retrospective study. Osteoporos Int 2021; 32 (11) 2323-2333
    CrossrefPubMedGoogle Scholar
  • 64 Otawa M, Tanoue R, Kido H, Sawa Y, Yamashita J. Intermittent administration of parathyroid hormone ameliorates periapical lesions in mice. J Endod 2015; 41 (05) 646-651
    CrossrefPubMedGoogle Scholar
  • 65 Lajla HB, Irmina T, Samra K, Aida D, Naida H. Root canal treatment modification at patient undergoing long-term bisphosphonate and cytostatic therapy. Stomatological Review/Stomatološki Vjesnik 2020;9(02):
    Google Scholar
  • 66 Segura-Egea JJ, Cabanillas-Balsera D, Martín-González J, Cintra LTA. Impact of systemic health on treatment outcomes in endodontics. Int Endod J 2023; 56 (Suppl. 02) 219-235
    CrossrefPubMedGoogle Scholar