58 Journal of Dental Implants | Jan - Jun 2013 | Vol 3 | Issue 1
Bacteria and dental implants: A review
Aravind Buddula ABSTRACT Dental implants have been shown to be an excellent method for replacing natural teeth. Dental implants like natural teeth can be affected by microorganisms. Various terms have been proposed to describe inflammation around dental implant. The ones that are commonly used include periimplantitis and periimplant mucositis. Studies were conducted that described the bacteriology of dental implants. Most studies reported that the microbiota associated with stable implants is similar to the one seen in periodontal health. Similarly, bacteria associated with failing implants have also been studied. These studies predominantly showed that the bacteria associated with failing implant are similar to the ones seen in periodontal disease. One should be very cautious in placing dental implants in subjects with significant periodontal disease as there is a risk for failure. Implants are not immune for infections. The present review briefly describes the bacteriology associated with stable and failing implants. KEY WORDS: Bacteria, implants, periimplantitis INTRODUCTION Dental implants like natural teeth are colonized by microorganisms. There are various terminologies associated with ailing and failing implants. Terms such as periimplant disease, periimplant mucositis, and periimplantitis have been proposed that describe pathologic conditions around dental implants. Dental implants are being used more frequently to restore partially edentulous or completely edentulous patients. Clinicians now are facing problems that they encountered with natural teeth. Like natural teeth dental implants are susceptible to infammation of the supporting tissues by colonization of pathogenic bacteria. Implant failure has been defined as the inadequacy of t he host t i ssue t o est abl i sh or mai nt ai n osseointegration. [1] Implant failures can be classifed based on the time of failure as early or late and based on the etiopathogenesis as infectious or noninfectious. [2,3] Early failures are due to failure to establish osseointegration and late failure is due to failure to maintain osseointegration. [4] Osseointegration is defined as a direct structural and functional connection between ordered living bone and surface of a loadcarrying implant. [5,6] Early failures can occur as a result of surgical trauma, premature loading of the implant, and bacterial infection. Late failures can occur following prosthetic rehabilitation. [2] Late failures can again be divided as soon late failures which occur during the frst year of loading and as delayed late failures occurring in subsequent years. Soon late failures can be attributed to overloading of the implant placed in bone that is poor both qualitatively and quantitatively. Delayed late failures can occur when there are changes in the loading conditions in relation to bone quality and volume and also as a result of periimplantitis. [2,7] The present review will focus on the microbiota associated with dental implants in healthy and diseased states. DEFINITION AND PREVALENCE OF PERIIMPLANT DISEASE European workshop on periodontology proposed the following definitions for inflammatory lesions that develop around implants. [8] Periimplant disease: The infammatory lesions that develop in the tissues around the implants 15640 Redmond Way, Redmond, USA Address for correspondence: Dr. Aravind Buddula, 15640 Redmond Way, Redmond, USA, E-mail: arvimayo@yahoo.com Access this article online Quick Response Code: Website: www.jdionline.org DOI: 10.4103/0974-6781.111698 REVIEW ARTICLE Buddula: Bacteria and dental implants Journal of Dental Implants | Jan - Jun 2013 | Vol 3 | Issue 1 59 Periimplant mucositis: Reversible inflammatory reaction in the soft tissues surrounding a functioning implant Periimplantitis: Infammatory reactions associated with loss of supporting bone around an implant in function. However, Zitzmann, et al. [9] provided new defnitions for these infammatory lesions. Periimplant Disease: Infammatory reactions in the tissues surrounding an implant Periimplant Mucositis: Presence of infammation in the mucosa at an implant with no signs of loss of supporting bone Periimplantitis: Presence of infammation and loss of supporting bone. Authors in their latest defnition eliminated the words reversible and irreversible proposed by the European workshop on periodontology as it might imply that the process cannot be treated. Authors were of the opinion that periimplantitis is treatable hence it cannot be considered irreversible. Periimplant mucositis is comparable to gingivitis around natural teeth as there is no loss of supporting structure and periimplantitis is comparable to periodontitis around natural teeth as there is bone loss associated with it. PREVALENCE OF PERIIMPLANT DISEASES There is the scant literature available about the prevalence of periimplant diseases. Crosssectional studies on prevalence of implant related disease are rare. Hence, there is a scarcity in the available literature about the prevalence of implant related diseases. Based on the available literature, periimplant mucositis occurred in approximately 80% of the subjects and in 50% of the implants. [10,11] Periimplantitis was identifed in 28% of the subjects and56% of subjects and in 12 and 43% of implant sites, respectively. [1014] MICROBIOTA AROUND HEALTHY AND DISEASED TEETH IN THE ABSENCE OF IMPLANTS Studies have shown that fora associated with healthy implants is similar to the fora in natural teeth and also that the fora associated with ailing/failing implants is similar to the one associated with periodontal disease. [1518] Hence, it is important for the clinician to evaluate the periodontal status of the subject before implant placement. Sampl es from heal thy gi ngi val sul cus consi st of predominantly grampositive anaerobic cocci and rods. Principally found are A. naeslundii, A. gerencseriae, S oralis, and Peptostreptococcus species which account for more than 50% of the bacteria. [1921] With the development of periodontitis, there are a higher proportion of gramnegative rods and decreased grampositive species. Increased proportions of P. gingivalis, B. forsythus and species of Prevotella, Fusobacterium, Campylobacter, and Treponema have been detected. [18,19] BACTERIOLOGY OF STABLE IMPLANTS There are only two longitudinal studies to date that report microbial colonization of stable dental implants. The frst study was done by Nakou, et al. [22] in 1987. They found that supragingival plaque in stable implants predominantly consists of grampositive cocci and subgingival plaque is dominated by Haemophilus spp and Veillonella parula. Second longitudinal study was done by Mombelli, et al. [23]
in 1988. They studied microbial colonization of ITI implants in edentulous patients. Samples were taken from periimplant crevice. They found that the fora was established shortly after installation of the dental implant. Over 85% of the organisms were identifed as coccoid cells and over 80% were grampositive facultative cocci. No, noteworthy, changes were found in the fora in the frst 6 months. Spirochetes were never detected and Fusobacteria and blackpigmenting gramnegative rods were found occasionally. Authors concluded from the study that bacteria around the implants in edentulous patients were similar to that found in the sulci of subjects with healthy periodontium. Mombelli, et al. [24] conducted a followup study in which they assess the microbial fora associated with stable osseointegrated dental implants. Majority of the patients were followed to the ffth year of implantation. No signifcant change was noted in the microbial fora during followup examinations. However, crosssectional studies are available in the literature that talks about bacteriology of stable implants. Lekholm, et al. [25] studied 20 patients with Brnemark implants. Mean observation time was 7.6 years. Coccoid and nonmotile rods dominated in up to 94% in the samples taken. Similarly, Apse, et al. [26] compared bacteriology of tooth and implant crevices. Microbiology included dark feld microscopy and anaerobic culturing. The results were interpreted by the authors as an indication that crevices around teeth may be reservoirs of bacteria for implant colonization. The authors were trying to explain higher percentages of black pigmenting anaerobes on implants in partially edentulous patients as opposed to completely edentulous patients. Rams, et al. [27] compared microbiota associated with osseointegrated hydroxyapatite coated titanium implants to pure titanium implants. No significant differences in the microbiota between the Buddula: Bacteria and dental implants 60 Journal of Dental Implants | Jan - Jun 2013 | Vol 3 | Issue 1 implant types. Strep. sanguis and Strep. mitis were the predominant organisms. Conclusions based on various studies about bacteriology of stable implants are as follows: Periimplant microbiota is established soon after implant placement Signifcant shifts in the fora do not occur over time Microfora is stable in healthy patients comprising a microbiota in which periodontal pathogens present only at low or below detectable levels. Composition of the subgingival microfora around implants in partially edentulous patients is a resultant of the composition of the fora around the teeth. Microbiota around failing implants Most studies reported that microbiota around failing dental implants harbored periodontopathic bacteria. Mombelli, et al. [17] reported data from seven cases with hollow cylinder titanium implants. Implant sites with pocket depth greater than 6 mm with bleeding on probing and suppuration were compared to successfully osseointegrated implants. Failing implants harbored a fora similar to adult periodontitis. Increased proportions of P. intermedia, Fusobacterium spp, and spirochetes were found around failing implants. Quirynen, et al. [28]
conducted a retrospective study with four Brnemark implants and four patients. Implants failing due to overload demonstrated flora similar to periodontal health and failing implants due to infection harbored periodontopathic flora. Rosenberg, et al. [29] studied 32 implants in subjects. This was a prospective study. Subjects were followed for 218 months. Implants failing due to infection had periodontopathic bacteria and implants failing due to traumatic infuences had fora similar to periodontal health. One study reported higher levels of P. gingivalis in failed implants. [30] Based on the observations from the abovementioned studies, it can be concluded that implants that fail due to infection have microbiota similar to those associated with periodontal disease. This could possibly be one of the reasons why implants fail more in subjects with periodontal disease compared to implants placed in otherwise healthy mouth. CONCLUSION A review of the literature so far leads to the conclusion that dental implants are not immune to infections. Like natural teeth, dental implants are colonized by bacteria. However there is a difference in the nature of microorganisms colonizing stable and failing implants. Most studies reported that stable implants have microbiota similar to that found in healthy periodontium. Grampositive anaerobic cocci and rods are the predominant species colonizing stable implants. In contrast, failing implants have bacteria similar to the ones seen in periodontal disease. This is based on the majority of the studies. Like any topic in periodontics, there are studies that refute these fndings. No matter what the studies show, it is wise to be cautious in placing dental implants in subjects with signifcant periodontal disease. It is important to treat the disease frst and then treatment plan for dental implants. REFERENCES 1. Heydenrijk K, Meijer HJ, Van der Reijden WA, Raghoebar GM, Vissink A, Stegenga B. Microbiota around root-form endosseous implants: A review of the literature. Int J Oral Maxillofac Implants 2002;17:829-38. 2. Esposito M, Hirsch JM, Lekholm U, Thomsen P. Biological factors contributing to failures of osseointegrated oral implants. Etiopathogenesis. Euro J Oral Sci 1998;106:721-64. 3. Buddula A, Assad DA, Salinas TJ, Garces YI, Volz JE, Weaver AL. Survival of dental implants in irradiated head and neck cancer patients: A retrospective analysis. Clin Imp Dent Relat Res 2012;14:716-22. 4. Tabanella G, Nowzari H, Slots J. Clinica and microbiological determinants of ailing dental implants. Clin Implant Dent Relat Research 2009;11:24-26. 5. Brnemerk PI. Introduction to osseointegration. In: Brnemark PI, editor. Tissue-integrated prosthesis: Osseointegration in clinical dentistry. Chicago, IL: Quintessence; 1985. p. 11-76. 6. Adell R, Lekholm U, Rockler B, Brnemark PI. A 15-year study of osseointegrated implants in the treatment of the edentulous jaw. Int J Ora Surg 1981;10:387-416. 7. Tonetti MS, Schmid J. Pathogenesis of implant failures. Periodontol 2000 1994;4:127-38. 8. Albrektsson T, Isidor F. Consensus report. In: Lang NP, Karring T, editors. Proceedings of the 1 st European workshop on periodontology; 1994. p. 365-9. 9. Zitzmann NU, Berglundh T. Defnition and prevalences of peri-implant diseases. J Clin Periodontol 2008;35:286-91. 10. Fransson C, Lekholm U, Jemt T, Berglundh T. Prevalence of subjects with progressive bone loss at implants. Clin Oral Implant Res 2005;16:440-6. 11. Fransson C, Wennstrom J, Berglundh T. Clinical characteristics at implants with a history of progressive bone loss. Clin Oral Implant Res 2008;19:142-7. 12. KaroussisIK,SalviGE,HeitzMayfeldL,BraggerJ,HammerleCH, Lang NP. Long-term implant prognosis in patients with and without a history of chronic periodontitis: A 10 year prospective cohort study of the ITI dental implant system. Clin Oral Implant Res 2003;14:329-39. 13. Roos-Jansaker AM, Lindahl C, Renvert H, Renvert S. Nine to Fourteen year follow-up of implant treatment. Part II: Presence of peri-implant lesions. J Clin Periodontol 2006;33:290-5. 14. Bragger U, Karaoussis I, Persson R, Pjetursson B, Salvi G, Lang N. Technical and biological complications/failures with singlecrownsandfxedpartialdenturesonimplants.A10year prospective cohort study. Clin Oral Implant Res 2005;16:326-34. 15. Quirynen M, Listgarten MA. Distribution of bacterial morphotypes around natural teeth and titanium implants ad modum Branemark. Clin Oral Implant Res 1990;1:8-12. 16. Apse P, Ellen RP, Overall CM, Zarb GA. Microbiota and crevicularfuidcollagenaseactivityintheosseointegrateddental implant sulcus: A comparison of sites in edentulous and partially edentulous patients. J Periodont Res 1989;24:96-105. 17. Mombelli A, Van Oosten MA, Schruch E Jr, Land NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiol Immunol 1987;2:145-51. Buddula: Bacteria and dental implants Journal of Dental Implants | Jan - Jun 2013 | Vol 3 | Issue 1 61 26. Apse P, Ellen RP, Overall CM, Zarb GA. Microbiota and crevicularfuidcollagenaseactivityintheosseointegrateddental implant sulcus: A comparison of sites in edentulous and partially edentulous patients. J Periodont Res 1989;24:96-105. 27. Rams TE, Link CC Jr. Microbiology of failing dental implants in humans: Electron microscopic observations. J Oral Implantol 1983;11:93-100. 28. Quirynen M, De Soete M, Dierickx K, Van Steenberghe D. The intra-oral translocations of periodontopathogens jeopardize the outcome of periodontal therapy. A review of the literature. J Clin Periodontol 2001;28:499-507. 29. Rosenberg ES, Torosian JP, Slots J. Microbial differences in 2 clinically distinct types of failures of osseointegrated implants. Clin Oral Implants Res 1991;2:135-44. 30. Van Winklehoff AJ, Goene RJ, Benshop C, Folmer T. Early colonization of dental implants by putative periodontal pathogens in partially edentulous patients. Clin Oral Implants Res 2000;11:511-20. 18. Meffert RM. Periodontitis and periimplantitis: One and the same? Pract Periodont Aesthetic Dent 1993;5:79-82. 19. SlotsJ.Microforainthehealthygingivalsulcusinman.Scand J Dent Res 1977;85:247-54. 20. Tanner A, Maiden MF, Macuch PJ, Murray LL, Kent RL Jr. Microbiota of health, gingivitis and initial periodontitis. J Clin Periodontol 1998;25:85-98. 21. Haffajee AD, Cugini MA, Tanner A, Pollack RP, Smith C Kent RL Jr, Socransky SS. Subgingival microbiota in healthy, well-maintained elder and periodontitis subjects. J Clin Periodontol 1998;25:346-53. 22. Nakou M, Mikx FH, Oosterwaal PJ, Kruijsen JC. Early microbial colonization of permucosal implants in edentulous patients. J Dent Res 1987;11:1654-7. 23. Mombelli A, Buser D, Lang NP. Colonization of osseointegrated titanium implants in edentulous patients. Early results. Oral Microbiol Immunol 1988;3:113-20. 24. Mombelli A, Mericske-Stern R. Microbiological features of stable osseointegrated implants used as abutments for overdentures. Clin Oral Impl Res 1990;1:1-7. 25. Lekholm U, Adell R, Lindhe J, Brnemark P, Eriksson B, Rockler B, et al. Marginal tissue reactions at Osseointegrated titaniumfxtures.Acrosssectionalretrospectivestudy.IntJOral Maxillofac Surg 1986;15:53-61. How to cite this article: Buddula A. Bacteria and dental implants: A review. J Dent Implant 2013;3:58-61. Source of Support: Nil, Confict of Interest: None. 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