Analysis of the association of IL1B(C-511T) polymorphism with dental implant loss and the clusterization phenomenon
Acir José Dirschnabel,
Fabiano Alvim-Pereira,
Cláudia Cristina Alvim-Pereira,
José Fábio Bernardino,
Edvaldo Antonio Ribeiro Rosa,
Paula Cristina Trevilatto,
Acir José Dirschnabel
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorFabiano Alvim-Pereira
Department of Dentistry, Center of Health Sciences,Universidade Federal de Sergipe (UFS), Aracaju, SE, Brazil
Search for more papers by this authorCláudia Cristina Alvim-Pereira
Department of Biophysics and Radiobiology, Center of Biologic Sciences, Universidade Federal de Pernambuco (UFPE), Recife, PE, Brazil
Search for more papers by this authorJosé Fábio Bernardino
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorEdvaldo Antonio Ribeiro Rosa
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorPaula Cristina Trevilatto
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorAcir José Dirschnabel,
Fabiano Alvim-Pereira,
Cláudia Cristina Alvim-Pereira,
José Fábio Bernardino,
Edvaldo Antonio Ribeiro Rosa,
Paula Cristina Trevilatto,
Acir José Dirschnabel
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorFabiano Alvim-Pereira
Department of Dentistry, Center of Health Sciences,Universidade Federal de Sergipe (UFS), Aracaju, SE, Brazil
Search for more papers by this authorCláudia Cristina Alvim-Pereira
Department of Biophysics and Radiobiology, Center of Biologic Sciences, Universidade Federal de Pernambuco (UFPE), Recife, PE, Brazil
Search for more papers by this authorJosé Fábio Bernardino
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorEdvaldo Antonio Ribeiro Rosa
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorPaula Cristina Trevilatto
Center for Health and Biological Sciences (CCBS), Pontifícia Universidade Católica do Paraná (PUCPR), Curitiba, PR, Brazil
Search for more papers by this authorCorresponding author:
Paula Cristina Trevilatto
Center for Health and Biological SciencesPontifícia Universidade Católica do Paraná (PUCPR)Rua Imaculada Conceição, 1155Curitiba, PR, CEP-80215-901BrazilTel.: +55 41 3271 2285Fax: +55 41 3271 1657e-mail: [email protected]
Abstract
Objectives: Endosteous dental implants consist in the treatment of choice to replace tooth loss. The knowledge that implant loss tends to cluster in subsets of individuals may indicate that host immune-inflammatory response is influenced by genetic factors. Interleukin-1 (IL-1) is a key mediator of inflammatory processes and functional polymorphisms in IL1 gene could be candidate genetic risk factors to study susceptibility to implant failure. The objective of this study was to investigate the association between IL1B (C-511T) genetic polymorphism and dental implant loss in a Brazilian population and its influence in the clusterization phenomenon.
Material and methods: The sample composed of 277 unrelated, both gender, mean age 53.63 ± 11.14 years individuals, divided into test group – 92 subjects with implant loss, and control group – 185 subjects with no implant loss. Patients' socioeconomic profile and clinical variables were investigated. Genomic DNA from oral mucosa was analyzed by polymerase chain reaction–restriction fragment length polymorphism.
Results: There was significant difference between the groups in medical treatment (P=0.040), edentulism (P=0.019), and mean number of placed implants (P=0.001). There was difference between groups with and without implant loss neither considering genotypes (P=0.279) nor alleles (P=0.168) for IL1B (C-511T) polymorphism. When individuals showing up to one implant failure (n=254) were investigated vs. patients presenting multiple implant loss (n=23), no difference was either observed between groups for genotype (P=0.083) and allele (P=0.838) frequencies.
Conclusions: The borderline association of the study polymorphism with implant loss suggests further IL1 haplotype analysis to elucidate the global involvement of IL-1 proteins in the modulation of the osseointegration process.
To cite this article: Dirschnabel AJ, Alvim-Pereira F, Alvim-Pereira CC, Bernardino JF, Rosa EAR, Trevilatto PC. Analysis of the association of IL1B(C-511T) polymorphism with dental implant loss and the clusterization phenomenon.Clin. Oral Impl. Res. 22, 2011; 1235–1241doi: 10.1111/j.1600-0501.2010.02080.x
References
- Aidar, M. & Line, S.R. (2007) A simple and cost-effective protocol for DNA isolation from buccal epithelial cells. Brazilian Dental Journal 18: 148–152.
- Alvim-Pereira, F., Montes, C.C., Mira, M.T. & Trevilatto, P.C. (2008) Genetic susceptibility to dental implant failure: a critical review. The International Journal of Oral & Maxillofacial Implants 23: 409–416.
- Apse, P., Ellen, R.P., Overall, C.M. & Zarb, G.A. (1989) Microbiota and crevicular fluid collagenase activity in the osseointegrated dental implant sulcus: a comparison of sites in edentulous and partially edentulous patients. Journal of Periodontal Research 24: 96–105.
- Baig, M.R. & Rajan, M. (2007) Effects of smoking on the outcome of implant treatment: a literature review. Indian Journal of Dental Research 18: 190–195.
- Birkedal-Hansen, H. (1993) Role of cytokines and inflammatory mediators in tissue destruction. Journal of Periodontal Research 28: 500–510.
- Boyce, B.F. & Xing, L. (2007) Biology of rank, rankl, and osteoprotegerin. Arthritis Research Therapy 9 (Suppl. 1): 51–58.
- Camargo, J.F., Correa, P.A., Castiblanco, J. & Anaya, J.M. (2004) Interleukin-1beta polymorphisms in Colombian patients with autoimmune rheumatic diseases. Genes Immunity 5: 609–614.
- Campos, M.I., Santos, M.C., Trevilatto, P.C., Scarel-Caminaga, R.M., Bezerra, F.J. & Line, S.R. (2005) Evaluation of the relationship between interleukin-1 gene cluster polymorphisms and early implant failure in non-smoking patients. Clinical Oral Implants Research 16: 194–201.
- Cargill, M., Altshuler, D., Ireland, J., Sklar, P., Ardlie, K., Patil, N., Shaw, N., Lane, C.R., Lim, E.P., Kalyanaraman, N., Nemesh, J., Ziaugra, L., Friedland, L., Rolfe, A., Warrington, J., Lipshutz, R., Daley, G.Q. & Lander, E.S. (1999) Characterization of single-nucleotide polymorphisms in coding regions of human genes. Nature Genetics 22: 231–238.
- Chen, H., Wilkins, L.M., Aziz, N., Cannings, C., Wyllie, D.H., Bingle, C., Rogus, J., Beck, J.D., Offenbacher, S., Cork, M.J., Rafie-Kolpin, M., Hsieh, C.M., Kornman, K.S. & Duff, G.W. (2006) Single nucleotide polymorphisms in the human interleukin-1b gene affect transcription according to haplotype context. Human Molecular Genetics 15: 519–529.
- Doundoulakis, J.H., Eckert, S.E., Lindquist, C.C. & Jeffcoat, M.K. (2003) The implant-supported overdenture as an alternative to the complete mandibular denture. The Journal of American Dental Association 134: 1455–1458.
- Ellen, R.P. (1998) Microbial colonization of the peri-implant environment and its relevance to long-term success of osseointegrated implants. International Journal of Prosthodontics 11: 433–441.
- Esposito, M., Grusovin, M.G., Maghaireh, H., Coulthard, P. & Worthington, H.V. (2007) Interventions for replacing missing teeth: management of soft tissues for dental implants. The Cochrane Database of Systematic Reviews CD006697.
- Esposito, M., Hirsch, J.M., Lekholm, U. & Thomsen, P. (1998) Biological factors contributing to failures of osseointegrated oral implants. (ii). Etiopathogenesis. European Journal of Oral Sciences 106: 721–764.
- Feloutzis, A., Lang, N.P., Tonetti, M.S., Burgin, W., Bragger, U., Buser, D., Duff, G.W. & Kornman, K.S. (2003) Il-1 gene polymorphism and smoking as risk factors for peri-implant bone loss in a well-maintained population. Clinical Oral Implants Research 14: 10–17.
- Greene, J.C. & Vermillion, J.R. (1964) The simplified oral hygiene index. The Journal of American Dental Association 68: 7–13.
- Greenstein, G. & Hart, T.C. (2002) A critical assessment of interleukin-1 (il-1) genotyping when used in a genetic susceptibility test for severe chronic periodontitis. Journal of Periodontology 73: 231–247.
- Gruica, B., Wang, H.Y., Lang, N.P. & Buser, D. (2004) Impact of il-1 genotype and smoking status on the prognosis of osseointegrated implants. Clinical Oral Implants Research 15: 393–400.
- Harada, Y., Watanabe, S., Yssel, H. & Arai, K. (1996) Factors affecting the cytokine production of human t cells stimulated by different modes of activation. Journal of Allergy and Clinical Immunology 98: S161–S173.
- Henry, P.J. (2005) Oral implant restoration for enhanced oral function. Clinical and Experimental Pharmacology and Physiology 32: 123–127.
- Holm-Pedersen, P., Lang, N.P. & Muller, F. (2007) What are the longevities of teeth and oral implants? Clinical Oral Implants Research 18 (Suppl. 3): 15–19.
- Jansson, H., Hamberg, K., De Bruyn, H. & Bratthall, G. (2005) Clinical consequences of il-1 genotype on early implant failures in patients under periodontal maintenance. Clinical Implant Dentistry and Related Research 7: 51–59.
- Karoussis, I.K., Kotsovilis, S. & Fourmousis, I. (2007) A comprehensive and critical review of dental implant prognosis in periodontally compromised partially edentulous patients. Clinical Oral Implants Research 18: 669–679.
- Khoury, S.B., Thomas, L., Walters, J.D., Sheridan, J.F. & Leblebicioglu, B. (2008) Early wound healing following one-stage dental implant placement with and without antibiotic prophylaxis: a pilot study. Journal of Periodontology 79: 1904–1912.
- Klemetti, E. (2008) Is there a certain number of implants needed to retain an overdenture? Journal of Oral Rehabilitation 35 (Suppl. 1): 80–84.
- Laine, M.L., Leonhardt, A., Roos-Jansaker, A.M., Pena, A.S., van Winkelhoff, A.J., Winkel, E.G. & Renvert, S. (2006) Il-1rn gene polymorphism is associated with peri-implantitis. Clinical Oral Implants Research 17: 380–385.
- Levin, L. (2008) Dealing with dental implant failures. Journal of Applied Oral Science 16: 171–175.
- Lin, Y.H., Huang, P., Lu, X., Guan, D.H., Man, Y., Wei, N., Wang, Y.Y. & Gong, P. (2007) The relationship between il-1 gene polymorphism and marginal bone loss around dental implants. Journal of Oral Maxillofacial Surgery 65: 2340–2344.
- Loe, H. & Silness, J. (1963) Periodontal disease in pregnancy. 1. Prevalence and severity. Acta Odontologica Scandinavica 21: 533–551.
- McDermott, N.E., Chuang, S.K., Woo, V.V. & Dodson, T.B. (2003) Complications of dental implants: identification, frequency, and associated risk factors. The International Journal of Oral & Maxillofacial Implants 18: 848–855.
- McDowell, T.L., Symons, J.A., Ploski, R., Forre, O. & Duff, G.W. (1995) A genetic association between juvenile rheumatoid arthritis and a novel interleukin-1 alpha polymorphism. Arthritis & Rheumatism 38: 221–228.
-
Mombelli, A. &
Cionca, N. (2006) Systemic diseases affecting osseointegration therapy.
Clinical Oral Implants Research
17
(Suppl. 2): 97–103.
10.1111/j.1600-0501.2006.01354.x Google Scholar
- Montes, C.C., Alvim-Pereira, F., de Castilhos, B.B., Sakurai, M.L., Olandoski, M. & Trevilatto, P.C. (2009) Analysis of the association of il1b (c+3954t) and il1rn (intron 2) polymorphisms with dental implant loss in a brazilian population. Clinical Oral Implants Research 20: 208–217.
- Montes, C.C., Pereira, F.A., Thome, G., Alves, E.D., Acedo, R.V., de Souza, J.R., Melo, A.C. & Trevilatto, P.C. (2007) Failing factors associated with osseointegrated dental implant loss. Implant Dentistry 16: 404–412.
- Muhle, R., Trentacoste, S.V. & Rapin, I. (2004) The genetics of autism. Pediatrics 113: e472–e486.
- Muraki, Y., Tsutsumi, A., Takahashi, R., Suzuki, E., Hayashi, T., Chino, Y., Goto, D., Matsumoto, I., Murata, H., Noguchi, E. & Sumida, T. (2004) Polymorphisms of il-1 beta gene in japanese patients with sjogren's syndrome and systemic lupus erythematosus. The Journal of Rheumatology 31: 720–725.
- Neukam, F.W. & Flemmig, T.F. (2006) Local and systemic conditions potentially compromising osseointegration. Consensus report of working group 3. Clinical Oral Implants Research 17 (Suppl. 2): 160–162.
- Nikolopoulos, G.K., Dimou, N.L., Hamodrakas, S.J. & Bagos, P.G. (2008) Cytokine gene polymorphisms in periodontal disease: a meta-analysis of 53 studies including 4178 cases and 4590 controls. Journal of Clinical Periodontology 35: 754–767.
- Nowzari, H., Yi, K., Chee, W. & Rich, S.K. (2008) Immunology, microbiology, and virology following placement of nobelperfect scalloped dental implants: analysis of a case series. Clinical Implant Dentistry and Related Research 10: 157–165.
- Panagakos, F.S., Aboyoussef, H., Dondero, R. & Jandinski, J.J. (1996) Detection and measurement of inflammatory cytokines in implant crevicular fluid: a pilot study. The International Journal of Oral & Maxillofacial Implants 11: 794–799.
- Papapanou, P.N., Neiderud, A.M., Sandros, J. & Dahlen, G. (2001) Interleukin-1 gene polymorphism and periodontal status. A case–control study. Journal of Clinical Periodontology 28: 389–396.
- Parks, C.G., Cooper, G.S., Dooley, M.A., Treadwell, E.L., St Clair, E.W., Gilkeson, G.S. & Pandey, J.P. (2004) Systemic lupus erythematosus and genetic variation in the interleukin 1 gene cluster: a population based study in the southeastern United States. Annals of the Rheumatic Diseases 63: 91–94.
- Parra, F.C., Amado, R.C., Lambertucci, J.R., Rocha, J., Antunes, C.M. & Pena, S.D. (2003) Color and genomic ancestry in Brazilians. Proceedings of the National Academy of Sciences of the United States of America 100: 177–182.
- Perala, D.G., Chapman, R.J., Gelfand, J.A., Callahan, M.V., Adams, D.F. & Lie, T. (1992) Relative production of il-1 beta and tnf alpha by mononuclear cells after exposure to dental implants. Journal of Periodontology 63: 426–430.
- Pietrowski, D., Thewes, R., Sator, M., Denschlag, D., Keck, C. & Tempfer, C. (2009) Uterine leiomyoma is associated with a polymorphism in the interleukin 1-beta gene. American Journal of Reproductive Immunology 62: 112–117.
- Pimenta, J.R., Zuccherato, L.W., Debes, A.A., Maselli, L., Soares, R.P., Moura-Neto, R.S., Rocha, J., Bydlowski, S.P. & Pena, S.D. (2006) Color and genomic ancestry in Brazilians: a study with forensic microsatellites. Human Heredity 62: 190–195.
- Pociot, F., Molvig, J., Wogensen, L., Worsaae, H. & Nerup, J. (1992) A taqi polymorphism in the human interleukin-1 beta (il-1 beta) gene correlates with il-1 beta secretion in vitro. European Journal of Clinical Investigation 22: 396–402.
- Quirynen, M., De Soete, M. & van Steenberghe, D. (2002) Infectious risks for oral implants: a review of the literature. Clinical Oral Implants Research 13: 1–19.
- Rechcinski, T., Grebowska, A., Kurpesa, M., Sztybrych, M., Peruga, J.Z., Trzos, E., Rudnicka, W., Krzeminska-Pakula, M. & Chmiela, M. (2009) Interleukin-1b and interleukin-1 receptor inhibitor gene cluster polymorphisms in patients with coronary artery disease after percutaneous angioplasty or coronary artery bypass grafting. Kardiologia polska 67: 601–610.
- Rogers, M.A., Figliomeni, L., Baluchova, K., Tan, A.E., Davies, G., Henry, P.J. & Price, P. (2002) Do interleukin-1 polymorphisms predict the development of periodontitis or the success of dental implants? Journal of Periodontal Research 37: 37–41.
- Rogus, J., Beck, J.D., Offenbacher, S., Huttner, K., Iacoviello, L., Latella, M.C., de Gaetano, M., Wang, H.Y., Kornman, K.S. & Duff, G.W. (2008) Il1b gene promoter haplotype pairs predict clinical levels of interleukin-1beta and c-reactive protein. Human Genetics 123: 387–398.
- Sadowsky, S.J. (2001) Mandibular implant-retained overdentures: a literature review. The Journal of Prosthetic Dentistry 86: 468–473.
- Salcetti, J.M., Moriarty, J.D., Cooper, L.F., Smith, F.W., Collins, J.G., Socransky, S.S. & Offenbacher, S. (1997) The clinical, microbial, and host response characteristics of the failing implant. The International Journal of Oral & Maxillofacial Implants 12: 32–42.
- Santos, M.C., Campos, M.I., Souza, A.P., Trevilatto, P.C. & Line, S.R. (2004) Analysis of mmp-1 and mmp-9 promoter polymorphisms in early osseointegrated implant failure. The International Journal of Oral & Maxillofacial Implants 19: 38–43.
- Schutte, B.C. & Murray, J.C. (1999) The many faces and factors of orofacial clefts. Human Molecular Genetics 8: 1853–1859.
- Serino, G. & Strom, C. (2009) Peri-implantitis in partially edentulous patients: association with inadequate plaque control. Clinical Oral Implants Research 20: 169–174.
- Shimpuku, H., Nosaka, Y., Kawamura, T., Tachi, Y., Shinohara, M. & Ohura, K. (2003) Genetic polymorphisms of the interleukin-1 gene and early marginal bone loss around endosseous dental implants. Clinical Oral Implants Research 14: 423–429.
- Silness, J. & Loe, H. (1964) Periodontal disease in pregnancy. 2. Correlation between oral hygiene and periodontal condition. Acta Odontologica Scandinavica 22: 121–135.
- Trevilatto, P.C. & Line, S.R. (2000) Use of buccal epithelial cells for pcr amplification of large DNA fragments. Journal of Forensic Odontostomatology 18: 6–9.
- Venter, J.C., Adams, M.D., Myers, E.W., Li, P.W., Mural, R.J., Sutton, G.G., Smith, H.O., Yandell, M., Evans, C.A., Holt, R.A., Gocayne, J.D., Amanatides, P., Ballew, R.M., Huson, D.H., Wortman, J.R., Zhang, Q., Kodira, C.D., Zheng, X.H., Chen, L., Skupski, M., Subramanian, G., Thomas, P.D., Zhang, J., Gabor Miklos, G.L., Nelson, C., Broder, S., Clark, A.G., Nadeau, J., McKusick, V.A., Zinder, N., Levine, A.J., Roberts, R.J., Simon, M., Slayman, C., Hunkapiller, M., Bolanos, R., Delcher, A., Dew, I., Fasulo, D., Flanigan, M., Florea, L., Halpern, A., Hannenhalli, S., Kravitz, S., Levy, S., Mobarry, C., Reinert, K., Remington, K., Abu-Threideh, J., Beasley, E., Biddick, K., Bonazzi, V., Brandon, R., Cargill, M., Chandramouliswaran, I., Charlab, R., Chaturvedi, K., Deng, Z., Di Francesco, V., Dunn, P., Eilbeck, K., Evangelista, C., Gabrielian, A.E., Gan, W., Ge, W., Gong, F., Gu, Z., Guan, P., Heiman, T.J., Higgins, M.E., Ji, R.R., Ke, Z., Ketchum, K.A., Lai, Z., Lei, Y., Li, Z., Li, J., Liang, Y., Lin, X., Lu, F., Merkulov, G.V., Milshina, N., Moore, H.M., Naik, A.K., Narayan, V.A., Neelam, B., Nusskern, D., Rusch, D.B., Salzberg, S., Shao, W., Shue, B., Sun, J., Wang, Z., Wang, A., Wang, X., Wang, J., Wei, M., Wides, R., Xiao, C., Yan, C., Yao, A., Ye, J., Zhan, M., Zhang, W., Zhang, H., Zhao, Q., Zheng, L., Zhong, F., Zhong, W., Zhu, S., Zhao, S., Gilbert, D., Baumhueter, S., Spier, G., Carter, C., Cravchik, A., Woodage, T., Ali, F., An, H., Awe, A., Baldwin, D., Baden, H., Barnstead, M., Barrow, I., Beeson, K., Busam, D., Carver, A., Center, A., Cheng, M.L., Curry, L., Danaher, S., Davenport, L., Desilets, R., Dietz, S., Dodson, K., Doup, L., Ferriera, S., Garg, N., Gluecksmann, A., Hart, B., Haynes, J., Haynes, C., Heiner, C., Hladun, S., Hostin, D., Houck, J., Howland, T., Ibegwam, C., Johnson, J., Kalush, F., Kline, L., Koduru, S., Love, A., Mann, F., May, D., McCawley, S., McIntosh, T., McMullen, I., Moy, M., Moy, L., Murphy, B., Nelson, K., Pfannkoch, C., Pratts, E., Puri, V., Qureshi, H., Reardon, M., Rodriguez, R., Rogers, Y.H., Romblad, D., Ruhfel, B., Scott, R., Sitter, C., Smallwood, M., Stewart, E., Strong, R., Suh, E., Thomas, R., Tint, N.N., Tse, S., Vech, C., Wang, G., Wetter, J., Williams, S., Williams, M., Windsor, S., Winn-Deen, E., Wolfe, K., Zaveri, J., Zaveri, K., Abril, J.F., Guigo, R., Campbell, M.J., Sjolander, K.V., Karlak, B., Kejariwal, A., Mi, H., Lazareva, B., Hatton, T., Narechania, A., Diemer, K., Muruganujan, A., Guo, N., Sato, S., Bafna, V., Istrail, S., Lippert, R., Schwartz, R., Walenz, B., Yooseph, S., Allen, D., Basu, A., Baxendale, J., Blick, L., Caminha, M., Carnes-Stine, J., Caulk, P., Chiang, Y.H., Coyne, M., Dahlke, C., Mays, A., Dombroski, M., Donnelly, M., Ely, D., Esparham, S., Fosler, C., Gire, H., Glanowski, S., Glasser, K., Glodek, A., Gorokhov, M., Graham, K., Gropman, B., Harris, M., Heil, J., Henderson, S., Hoover, J., Jennings, D., Jordan, C., Jordan, J., Kasha, J., Kagan, L., Kraft, C., Levitsky, A., Lewis, M., Liu, X., Lopez, J., Ma, D., Majoros, W., McDaniel, J., Murphy, S., Newman, M., Nguyen, T., Nguyen, N., Nodell, M., Pan, S., Peck, J., Peterson, M., Rowe, W., Sanders, R., Scott, J., Simpson, M., Smith, T., Sprague, A., Stockwell, T., Turner, R., Venter, E., Wang, M., Wen, M., Wu, D., Wu, M., Xia, A., Zandieh, A. & Zhu, X. (2001) The sequence of the human genome. Science 291: 1304–1351.
- Vincenzi, B., Patti, G., Galluzzo, S., Pantano, F., Venditti, O., Santini, D., Ruzzo, A., Schiavon, G., Caraglia, M., Marra, M., Graziano, F. & Tonini, G. (2008) Interleukin 1beta-511t gene (il1beta) polymorphism is correlated with gastric cancer in the Caucasian population: results from a meta-analysis. Oncology Reports 20: 1213–1220.
- Weyant, R.J. & Burt, B.A. (1993) An assessment of survival rates and within-patient clustering of failures for endosseous oral implants. Journal of Dental Research 72: 2–8.
- Wilson, T.G. Jr & Nunn, M. (1999) The relationship between the interleukin-1 periodontal genotype and implant loss. Initial data. Journal of Periodontology 70: 724–729.
- Wright, H.L., McCarthy, H.S., Middleton, J. & Marshall, M.J. (2009) Rank, rankl and osteoprotegerin in bone biology and disease. Current Reviews in Musculoskeletal Medicine 2: 56–64.
Citing Literature
