Oral microbiota and host innate immune response in bisphosphonate-related osteonecrosis of the jaw

Smruti Pushalkar , Xin Li , Zoya Kurago , Lalitha V Ramanathapuram , Satoko Matsumura , Kenneth E Fleisher , Robert Glickman , Wenbo Yan , Yihong Li , Deepak Saxena

International Journal of Oral Science ›› 2014, Vol. 6 ›› Issue (4) : 219 -226.

PDF
International Journal of Oral Science ›› 2014, Vol. 6 ›› Issue (4) : 219 -226. DOI: 10.1038/ijos.2014.46
Article

Oral microbiota and host innate immune response in bisphosphonate-related osteonecrosis of the jaw

Author information +
History +
PDF

Abstract

Decreased immune response and colonization by certain bacteria may increase risk of bisphosphonate-related osteonecrosis of the jaw (BRONJ). Deepak Saxena of the New York University College of Dentistry, USA, and colleagues have shown that cancer patients who have been treated with bisphosphonates to reduce bone loss can, paradoxically, experience localized bone loss from the jaw. In a study of 30 oral surgery patients, Saxena and colleagues used a genetic approach to identify oral bacteria in BRONJ lesions and compared the immune responses of BRONJ patients and controls. BRONJ patients showed decreased immune response and more frequent colonization by opportunistic pathogens such as Parvimonas, Fusobacterium, Eubacterium besides, Streptococcus onto the BP-bound bone contributing to jaw necrosis. Some unnamed or uncultured bacteria were only found in BRONJ and bisphosphonate-treated patients. This study of the relationship between microbial colonization and immune response provides insights into the disease process in BRONJ.

Keywords

bisphosphonates / denaturing gradient gel electrophoresis / host response / innate immunity / oral microbiota / osteonecrosis of the jaw

Cite this article

Download citation ▾
Smruti Pushalkar, Xin Li, Zoya Kurago, Lalitha V Ramanathapuram, Satoko Matsumura, Kenneth E Fleisher, Robert Glickman, Wenbo Yan, Yihong Li, Deepak Saxena. Oral microbiota and host innate immune response in bisphosphonate-related osteonecrosis of the jaw. International Journal of Oral Science, 2014, 6(4): 219-226 DOI:10.1038/ijos.2014.46

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ruggiero SL, Dodson TB, Assael LA. American Association of Oral and Maxillofacial Surgeons position paper on bisphosphonate-related osteonecrosis of the jaws—2009 update. J Oral Maxillofac Surg, 2009, 67(5 Suppl): 2-12.

[2]

Reid IR, Cornish J. Epidemiology and pathogenesis of osteonecrosis of the jaw. Nat Rev Rheumatol, 2012, 8(2): 90-96.

[3]

Hoefert S, Schmitz I, Tannapfel A. Importance of microcracks in etiology of bisphosphonate-related osteonecrosis of the jaw: a possible pathogenetic model of symptomatic and non-symptomatic osteonecrosis of the jaw based on scanning electron microscopy findings. Clin Oral Investig, 2010, 14(3): 271-284.

[4]

Saia G, Blandamura S, Bettini G. Occurrence of bisphosphonate-related osteonecrosis of the jaw after surgical tooth extraction. J Oral Maxillofac Surg, 2010, 68(4): 797-804.

[5]

Ruggiero S, Gralow J, Marx RE. Practical guidelines for the prevention, diagnosis, and treatment of osteonecrosis of the jaw in patients with cancer. J Oncol Pract, 2006, 2(1): 7-14.

[6]

Migliorati CA, Schubert MM, Peterson DE. Bisphosphonate-associated osteonecrosis of mandibular and maxillary bone: an emerging oral complication of supportive cancer therapy. Cancer, 2005, 104(1): 83-93.

[7]

Fedele S, Kumar N, Davies R. Dental management of patients at risk of osteochemonecrosis of the jaws: a critical review. Oral Dis, 2009, 15(8): 527-537.

[8]

Diz P, Limeres J, Fedele S. Is oral bisphosphonate-related osteonecrosis of the jaw an endemic condition. Med Hypotheses, 2012, 78(2): 315-318.

[9]

Filleul O, Crompot E, Saussez S. Bisphosphonate-induced osteonecrosis of the jaw: a review of 2,400 patient cases. J Cancer Res Clin Oncol, 2010, 136(8): 1117-1124.

[10]

Kos M, Brusco D, Kuebler J. Clinical comparison of patients with osteonecrosis of the jaws, with and without a history of bisphosphonates administration. Int J Oral Maxillofac Surg, 2010, 39(11): 1097-1102.

[11]

Baur DA, Weber JM, Collette DC. Osteonecrosis of the jaws unrelated to bisphosphonate exposure: a series of 4 cases. J Oral Maxillofac Surg, 2012, 70(12): 2802-2808.

[12]

Ikebe T. Pathophysiology of BRONJ: drug-related osteoclastic disease of the jaw. Oral Sci Int, 2013, 10(1): 1-8.

[13]

Infante-Cossio P, Lopez-Martin JC, Gonzalez-Cardero E. Osteonecrosis of the maxilla associated with cancer chemotherapy in patients wearing dentures. J Oral Maxillofac Surg, 2012, 70(7): 1587-1592.

[14]

Pazianas M. Osteonecrosis of the jaw and the role of macrophages. J Natl Cancer Inst, 2011, 103(3): 232-240.

[15]

Sivolella S, Lumachi F, Stellini E. Denosumab and anti-angiogenetic drug-related osteonecrosis of the jaw: an uncommon but potentially severe disease. Anticancer Res, 2013, 33(5): 1793-1797.

[16]

Allen MR, Burr DB. The pathogenesis of bisphosphonate-related osteonecrosis of the jaw: so many hypotheses, so few data. J Oral Maxillofac Surg, 2009, 67(5 Suppl): 61-70.

[17]

Goda A1, Maruyama F, Michi Y. Analysis of the factors affecting the formation of the microbiome associated with chronic osteomyelitis of the jaw. Clin Microbiol Infect, 2014, 20(5): O309-O317.

[18]

Hoefert S, Eufinger H. Relevance of a prolonged preoperative antibiotic regime in the treatment of bisphosphonate-related osteonecrosis of the jaw. J Oral Maxillofac Surg, 2011, 69(2): 362-380.

[19]

Ji X, Pushalkar S, Li Y. Antibiotic effects on bacterial profile in osteonecrosis of the jaw. Oral Dis, 2012, 18(1): 85-95.

[20]

Kumar SK, Gorur A, Schaudinn C. The role of microbial biofilms in osteonecrosis of the jaw associated with bisphosphonate therapy. Curr Osteoporos Rep, 2010, 8(1): 40-48.

[21]

Lesclous P, Abi Najm S, Carrel JP. Bisphosphonate-associated osteonecrosis of the jaw: a key role of inflammation. Bone, 2009, 45(5): 843-852.

[22]

Reid IR. Osteonecrosis of the jaw: who gets it, and why. Bone, 2009, 44(1): 4-10.

[23]

Wolf AM, Rumpold H, Tilg H. The effect of zoledronic acid on the function and differentiation of myeloid cells. Haematologica, 2006, 91(9): 1165-1171.

[24]

Wei X, Pushalkar S, Estilo C. Molecular profiling of oral microbiota in jawbone samples of bisphosphonate-related osteonecrosis of the jaw. Oral Dis, 2012, 18(6): 602-612.

[25]

Abu-Id MH, Warnke PH, Gottschalk J. "Bis-phossy jaws" - high and low risk factors for bisphosphonate-induced osteonecrosis of the jaw. J Craniomaxillofac Surg, 2008, 36(2): 95-103.

[26]

Hansen T, Kunkel M, Weber A. Osteonecrosis of the jaws in patients treated with bisphosphonates—histomorphologic analysis in comparison with infected osteoradionecrosis. J Oral Pathol Med, 2006, 35(3): 155-160.

[27]

Kaplan I, Anavi K, Anavi Y. The clinical spectrum of Actinomyces-associated lesions of the oral mucosa and jawbones: correlations with histomorphometric analysis. Oral Surg Oral Med Oral Pathol Oral Radiol Endod, 2009, 108(5): 738-746.

[28]

Sedghizadeh PP, Kumar SK, Gorur A. Identification of microbial biofilms in osteonecrosis of the jaws secondary to bisphosphonate therapy. J Oral Maxillofac Surg, 2008, 66(4): 767-775.

[29]

Sedghizadeh PP, Kumar SK, Gorur A. Microbial biofilms in osteomyelitis of the jaw and osteonecrosis of the jaw secondary to bisphosphonate therapy. J Am Dent Assoc, 2009, 140(10): 1259-1265.

[30]

Li Y, Ge Y, Saxena D. Genetic profiling of the oral microbiota associated with severe early-childhood caries. J Clin Microbiol, 2007, 45(1): 81-87.

[31]

Pushalkar S, Ji X, Li Y. Comparison of oral microbiota in tumor and non-tumor tissues of patients with oral squamous cell carcinoma. BMC Microbiol, 2012, 12: 144.

[32]

DeSantis TZ, Hugenholtz P, Larsen N. Greengenes, a chimera-checked 16S rRNA gene database and workbench compatible with ARB. Appl Environ Microbiol, 2006, 72(7): 5069-5072.

[33]

Dewhirst FE, Chen T, Izard J. The human oral microbiome. J Bacteriol, 2010, 192(19): 5002-5017.

[34]

Roberts AP, Mullany P. Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev Anti Infect Ther, 2010, 8(12): 1441-1450.

[35]

Stewart PS, Costerton JW. Antibiotic resistance of bacteria in biofilms. Lancet, 2001, 358(9276): 135-138.

[36]

Sedghizadeh PP, Yooseph S, Fadrosh DW. Metagenomic investigation of microbes and viruses in patients with jaw osteonecrosis associated with bisphosphonate therapy. Oral Surg Oral Med Oral Pathol Oral Radiol, 2012, 114(6): 764-770.

[37]

Kolenbrander PE, Andersen RN, Blehert DS. Communication among oral bacteria. Microbiol Mol Biol Rev, 2002, 66(3): 486-505.

[38]

Arif N, Sheehy EC, Do T. Diversity of Veillonella spp. from sound and carious sites in children. J Dent Res, 2008, 87(3): 278-282.

[39]

Ota-Tsuzuki C, Alves Mayer MP. Collagenase production and hemolytic activity related to 16S rRNA variability among Parvimonas micra oral isolates. Anaerobe, 2010, 16(1): 38-42.

[40]

Hsiao WW, Li KL, Liu Z. Microbial transformation from normal oral microbiota to acute endodontic infections. BMC Genomics, 2012, 13: 345.

[41]

Gray T. Streptococcus anginosus group: clinical significance of an important group of pathogens. Clin Microbiol Newsl, 2005, 27(20): 155-159.

[42]

Downes J, Wade WG. Peptostreptococcus stomatis sp. nov., isolated from the human oral cavity. Int J Syst Evol Microbiol, 2006, 56(Pt 4): 751-754.

[43]

Nakazawa F, Miyakawa H, Fujita M. Significance of asaccharolytic Eubacterium and closely related bacterial species in the human oral cavity. J Exp Clin Med, 2011, 3(1): 17-21.

[44]

Salam MA, Sato M, Hoshino E. Intraperitoneal immune cell responses to Eubacterium saphenum in mice. Microbiol Immunol, 2001, 45(1): 29-37.

[45]

Gibbons RJ. Bacterial adhesion to oral tissues: a model for infectious diseases. J Dent Res, 1989, 68(5): 750-760.

[46]

Sedghizadeh PP, Jones AC, LaVallee C. Population pharmacokinetic and pharmacodynamic modeling for assessing risk of bisphosphonate-related osteonecrosis of the jaw. Oral Surg Oral Med Oral Pathol Oral Radiol, 2013, 115(2): 224-232.

[47]

Liu B, Faller LL, Klitgord N. Deep sequencing of the oral microbiome reveals signatures of periodontal disease. PLoS One, 2012, 7(6): e37919.

[48]

Loesche WJ. Bacterial mediators in periodontal disease. Clin Infect Dis, 1993, 16(Suppl 4): S203-S210.

[49]

Ganguli A, Steward C, Butler SL. Bacterial adhesion to bisphosphonate coated hydroxyapatite. J Mater Sci Mater Med, 2005, 16(4): 283-287.

[50]

Kos M, Luczak K. Bisphosphonates promote jaw osteonecrosis through facilitating bacterial colonisation. Biosci Hypotheses, 2009, 2(1): 34-36.

[51]

Perrotta I, Cristofaro MG, Amantea M. Jaw osteonecrosis in patients treated with bisphosphonates: an ultrastructural study. Ultrastruct Pathol, 2010, 34(4): 207-213.

[52]

Wanger G, Gorby Y, El-Naggar MY. Electrically conductive bacterial nanowires in bisphosphonate-related osteonecrosis of the jaw biofilms. Oral Surg Oral Med Oral Pathol Oral Radiol, 2013, 115(1): 71-78.

[53]

Kassolis JD, Scheper M, Jham B. Histopathologic findings in bone from edentulous alveolar ridges: a role in osteonecrosis of the jaws. Bone, 2010, 47(1): 127-130.

[54]

Leibovich SJ, Ross R. The role of the macrophage in wound repair. A study with hydrocortisone and antimacrophage serum. Am J Pathol, 1975, 78(1): 71-100.

[55]

Rappolee DA, Mark D, Banda MJ. Wound macrophages express TGF-alpha and other growth factors in vivo: analysis by mRNA phenotyping. Science, 1988, 241(4866): 708-712.

[56]

Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukoc Biol, 2005, 77(5): 598-625.

[57]

Raychaudhuri SP, Nguyen CT, Raychaudhuri SK. Incidence and nature of infectious disease in patients treated with anti-TNF agents. Autoimmun Rev, 2009, 9(2): 67-81.

[58]

Koziol-Montewka M, Magrys A, Paluch-Oles J. MPO and cytokines in the serum of cancer patients in the context of Candida colonization and infection. Immunol Invest, 2006, 35(2): 167-179.

[59]

Lipinski S, Till A, Sina C. DUOX2-derived reactive oxygen species are effectors of NOD2-mediated antibacterial responses. J Cell Sci, 2009, 122(Pt 19): 3522-3530.

[60]

Doumas S, Kolokotronis A, Stefanopoulos P. Anti-inflammatory and antimicrobial roles of secretory leukocyte protease inhibitor. Infect Immun, 2005, 73(3): 1271-1274.

[61]

Kessenbrock K, Fröhlich L, Sixt M. Proteinase 3 and neutrophil elastase enhance inflammation in mice by inactivating antiinflammatory progranulin. J Clin Invest, 2008, 118(7): 2438-2447.

[62]

Epstein JB, Stevenson-Moore P. Periodontal disease and periodontal management in patients with cancer. Oral Oncol, 2001, 37(8): 613-619.

[63]

Brunello A, Saia G, Bedogni A. Worsening of osteonecrosis of the jaw during treatment with sunitinib in a patient with metastatic renal cell carcinoma. Bone, 2009, 44(1): 173-175.

[64]

Kamada N, Seo SU, Chen GY. Role of the gut microbiota in immunity and inflammatory disease. Nat Rev Immunol, 2013, 13(5): 321-335.

[65]

Favot CL, Forster C, Glogauer M. The effect of bisphosphonate therapy on neutrophil function: a potential biomarker. Int J Oral Maxillofac Surg, 2013, 42(5): 619-626.

[66]

Henderson B, Nair SP. Hard labour: bacterial infection of the skeleton. Trends Microbiol, 2003, 11(12): 570-577.

AI Summary AI Mindmap
PDF

160

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/