Open access peer-reviewed chapter

Peri-implantitis Microbiota

Written By

Dalia Khalil and Margareta Hultin

Submitted: 04 March 2018 Reviewed: 13 June 2018 Published: 05 November 2018

DOI: 10.5772/intechopen.79486

Chapter metrics overview

1,332 Chapter Downloads

View Full Metrics


Dental implant surgery has been a successful therapeutic option for the rehabilitation of partially or completely edentulous jaws for many years. However, evidence regarding the causative factors of peri-implant disease is still lacking. Peri-implantitis is an inflammatory disease affecting the soft and hard tissues surrounding osseointegrated implant associated with the formation of a bacterial biofilm on the implant surface close to the marginal tissues. The aim of this chapter is to summarize the knowledge regarding the microbiota associated with peri-implant infection and to review the different microbial diagnostic tests to understand the peri-implant microbiota, as well as summarize the present knowledge regarding management of peri-implantitis and propose further recommendations for future studies. This chapter shows that the scientific data regarding the microbiota responsible for peri-implantitis initiation and progression are still inconclusive. A microbiological test may thus be one diagnostic method to be used to understand the complexity of microbiota associated with the peri-implant sulcus. However, in order to resolve inflammation and arrest disease progression, the understanding of the biofilm development is essential.


  • dental implant
  • peri-implant infection
  • peri-implantitis
  • peri-implant microbiota
  • peri-implant microbial test

1. Introduction

Dental implants have become a successful therapeutic option to replace missing tooth. It has been estimated that approximately 12 million implants are placed every year, worldwide [1]. With the global increase of dental implant placement, there is a continued need for investigation regarding the etiology, risk factors and treatment for dental implant complications. Moreover, the widespread use of dental implants has led to an increase in biofilm-mediated peri-implant disease. There is an undisputed effect between the formation of an oral biofilm on the implant surface and the initiation of the inflammatory process around osseointegrated dental implants [2].

Initially, clinical measures such as probing were not recommended since it was believed that this could harm the mucosal seal. Therefore, diagnostic measures were limited to the radiographic examination. Thus, disease remained undiagnosed for many years. Therefore, failing dental implants were not diagnosed, and only failed implants were detected where the implant needed to be removed [3]. First, the term peri-implantoclasia was used to describe the disease condition, that is, catabolic condition with/without sepsis or suppuration, around the dental implant [4, 5]. However, this term was replaced shortly after with peri-implantitis, which became the accepted terminology for the infectious nature of the pathologic condition surrounding peri-implant tissue [6, 7].

Peri-implantitis has been described as a “site specific” condition or as an “inflammatory bacterial driven destruction of the implant supporting apparatus,” which means that microorganisms play an important role in peri-implantitis [8, 9]. The prevalence of peri-implantitis shows a wide range (10-25%) in different study populations primarily due to the definition of peri-implantitis, i.e. the chosen cut-off level for registering marginal bone loss and the duration of the patient’s follow-up [10, 11]. However, one of the major challenges in the treatment of peri-implantitis is the lack of effective treatments.


2. Periodontitis versus peri-implantitis

Peri-implantitis is defined as an inflammatory disease affecting the soft and hard tissues surrounding osseointegrated functioning implants, while periodontitis is defined as inflammation affecting the tissues around the teeth [12, 13]. Despite the similarities between peri-implantitis and periodontitis, they seem to differ in extent, composition and progression of lesions [14, 15]. Peri-implant disease is known to be multifactorial with risk factors identical to periodontitis, including poor oral hygiene, smoking, diabetes, and genetic factors [2, 16]. History, or current periodontitis status, increases the risk of peri-implantitis [2, 16, 17, 18, 19]. However, there is a complex interaction between the development of periodontitis and peri-implantitis and the formation of bacterial biofilm [2, 16].

One of the major anatomical differences between periodontal and peri-implant tissue is the presence of a periodontal ligament around the tooth, while the implant is in an ankylosed state. Although there is extensive information regarding the histopathological characteristics of human periodontal lesions, only a few studies have evaluated peri-implantitis lesions in humans. Berglundh et al. concluded in a systematic review that critical histopathological differences exist between the two lesions [20]. For example, the apical extension of the inflammatory cell infiltrate was more pronounced in peri-implantitis lesions compared to that in periodontal lesions. In peri-implantitis, the inflammatory cell infiltrate was, in most cases, located apical of the pocket epithelium. In both types of lesions, the infiltrate was dominated by plasma cells and lymphocytes, but in peri-implantitis, the neutrophil granulocytes and macrophages occurred in larger proportions [20]. In a recent animal study on mice, where periodontitis and peri-implantitis lesions were experimentally induced by ligatures, a striking difference was observed on comparing the spontaneous healing after ligature removal. More bone was regained after ligature removal around teeth compared with that around implants in the peri-implantitis lesions. The intrinsic ability of the periodontal ligament to repair bone around teeth may thus be one of several key factors influencing treatment outcomes of peri-implantitis [21]. Moreover, soft tissues around teeth and implants are of similar dimensions [3]. The outer surface of the gingiva and peri-implant mucosa is covered by keratinized oral epithelium, but the peri-implant mucosa continues marginally with a thin nonkeratinized barrier epithelium, which is similar to the junctional epithelium around teeth [3]. However, the reaction of the soft and hard tissue after microbial colonization is similar in many aspects [3].

It was previously believed that there are similarities between peri-implantitis and periodontitis microbiota, and that periodontal pathogens translocate into peri-implant tissue. These similarities were once considered a critical factor in disease causation [19]. Recently, it has been reported that peri-implantitis and periodontitis microbial environments are distinct, with differences in core microbiota between the two conditions [20, 22, 23, 24].


3. Peri-implant microbiology

Implant insertion appears to stimulate the mechanism of mature biofilm development. However, this initially formed biofilm is in a commensal state [25, 26]. The biofilm that surrounds healthy implants is confined supramucosally, regardless of the fact that it can be found in massive amounts [27]. Bacterial colonization starts approximately 30 min after the implant is inserted into the oral environment [28, 29]. Recently, studies identified more than 700 bacterial species and 25,000 phylotypes in the oral cavity [22, 30, 31, 32].

The bacterial composition of the peri-implant biofilm harbors a similar microbiota to that of the neighboring teeth [33], which means that teeth serve as reservoirs for bacterial colonization in the biofilm surrounding implants [6, 34, 35, 36]. Similarities between peri-implant and periodontal microflora have been shown in several studies [37, 38, 39]. The subgingival microbiota of diseased implants has generally been considered to share some common characteristics [33].

The peri-implant microbiota of healthy sites has been shown in some studies to be more diverse and complex than in peri-implantitis, which indicates that healthy sites have a more stable and healthy ecosystem [40, 41]. On the other hand, other studies have shown higher microbiota diversity in diseased subjects [42]. These observations demonstrate that the microbial communities in both healthy and diseased tissue are quite different; however, generally, most taxa are present in both conditions [42, 43].

The subgingival microbiota of healthy implants and peri-implantitis are colonized by periodontopathic microorganisms [44, 45]. For example, the peri-implantitis microbiota showed up to a 40% higher frequency of red complex and orange complex compared to healthy implants [8, 44, 46, 47, 48, 49, 50, 51]. The most frequent periodontal pathogens presented in a peri-implantitis lesions are from genera such as Bacteroides, Prevotella, Porphyromonas, Treponema, and Tannerella [46, 52, 53, 54]. Moreover, there is an increase in the diversity of species in the more advanced stages of disease [51]. Previous studies suggest that periodontopathic bacteria are not the only periodontal pathogens active in peri-implantitis, and that noncultivable microorganisms such as asaccharolytic anaerobic Gram-positive rods (AAGPRs) and oxidized graphene nanoribbons (OGNRs) may also play an important role in peri-implantitis lesions [41, 44, 54, 55, 56, 57]. In addition, Gram-negative microorganisms such as Aggregatibacter actinomycetemcomitans (Aa), Parvimonas micra (Pm), and Campylobacter rectus (Cr) were identified in 52% of the studies [46, 48, 58, 59, 60, 61, 62, 63, 64, 65] presented in a systematic review by Lafaurie [44]. Few studies have shown the presence of Pseudomonas aeruginosa, Candida albicans, Staphylococcus aureus, and Staphylococcus Warneri in peri-implantitis lesions [46, 47, 66]. In addition, the Epstein-Barr virus has been considered an enhanced risk factor in peri-implantitis lesions [67, 68]. However, it is not yet considered a microbiologic marker for peri-implantitis [67, 68]. The role of phylum Synergistetes in peri-implantitis lesions is still debated. Some recent studies have shown a strong association between this phylum and the occurrence of peri-implantitis [69, 70], while others conclude there is no relationship [71]. Therefore, peri-implantitis lesions represent a heterogeneous infection [44].

There are many factors that determine the variation in peri-implant microbiota and also the degree of its shift from the healthy microbiota found in the peri-implant sulcus. These factors include differences in the microbiological detection methods used in various studies [45, 72]. Moreover, inter-individual variations in oral microbiota (such as the presence of pathologic conditions in the oral environment, for example, untreated periodontal disease, smokers, or the status of edentulous), study design (longitudinal or cross-sectional, number of participants), and how the samples are handled all influence variations between studies [14, 72, 73]. To date, there is still limited data on which bacteria are involved in the initiation and progression of peri-implantitis disease [15]. Therefore, we should emphasize the fact that regardless of the statistically significant changes in peri-implant microbiota, microbiome composition shows a high tendency for changes that lead to a shift from a healthy status to a diseased status [72].


4. Microbial diagnostic tests

To date, clinical and radiographic data are the main diagnostic methods for the diagnosis of peri-implant disease. However, these methods are limited because they only detect the disease after a certain level of destruction [45]. Therefore, the use of microbiological tests is important to be able to determine the microbiota associated with the peri-implant sulcus [45]. There are different ways of testing the bacterial composition at the peri-implant sites. First, the sample is collected using sterile paper points, a sterile periodontal probe or a curette. These samples are then analyzed either by culture-based methods, molecular methods, sequencing methods, or other advanced new methods (i.e., metagenomics).

Culture-based methods were the first approach in helping understanding the human microbiomes. However, 20–60% of the microbiome is known to be uncultivable [74]. The limitation of this technique is that it is both time-consuming, and the results underestimate the diversity of the human microbiota.

The molecular methods, such as PCR or DNA-DNA hybridization, help to increase the number of bacterial species known to be oral commensals, which leads to increased understanding of the disease process. These methods are faster and more sensitive than the culture-based ones, but are also limited because of the need to pre-select DNA probes for the specific bacterial taxa to be investigated [39]. Therefore, one has to be cautious when interpreting these results, as finding “unexpected” microbiota is impossible with these techniques, thus creating a risk of bias. However, these techniques have overcome the limitations of culturing techniques.

During the last few years, sequencing methods such as 16S rRNA have allowed the evaluation of an entire community’s microbiome [39, 57]. These methods use a universal primer system to detect a broad range of bacterial taxa [75, 76] and discover previously new undetected and uncultivable bacteria [41, 57, 70]. Sequencing methods are able to overcome the limitations of the above-mentioned methods. On the other hand, this technique also has limitations. For example, in determining differences at the strain level, some taxa may escape detection due to less effective primer binding or differential amplification [39, 72].

Recently, some studies have used metagenomic methods for investigating microbiomes. This method is based on extracting DNA directly from the sample without “looking for” a specific organism and can be randomly sequenced or functionally screened for activities of interest [77]. These methods have recently provided valuable insights into the pathogenesis of periodontitis and may allow a paradigm shift in the understanding of peri-implantitis disease. However, studies using this technique are still ongoing.


5. Management of peri-implantitis

To date, there is no clear evidence to indicate what the initiating factors for peri-implant disease are. However, microbial infections with bacteria and possibly yeasts and viruses play an important role in the disease process [16, 46, 78, 79]. Peri-implantitis is always considered an infectious disease with the need for antimicrobial treatment to empirically target specific putative bacteria [78, 80, 81, 82, 83, 84, 85, 86, 87]. The primary treatment goals of peri-implantitis are to resolve inflammation and arrest disease progression. Surface decontamination is important to consider during treatment. There is no gold standard in the treatment of peri-implantitis. However, surgical access with the adjunctive use of different chemical detergents, air powder abrasive devises or lasers have been previously presented to achieve surface decontamination [88].

Data regarding the effect of systematic antibiotics on peri-implantitis lesions are lacking long-term outcomes. Although the effect of systemic antimicrobials agents in the surgical treatment of peri-implantitis is still limited [38], time and dosage have made the risk of antibiotic resistance development a reality [78, 89]. Using antimicrobial agents may risk developing bacterial resistance and the overgrowth of superinfecting microorganisms that are difficult to eradicate [78]. The development of opportunistic pathogens, such as S. aureus or EBV, may lead to a change in the normal symbiotic ecosystem to a dysbiotic ecosystem by affecting the local innate immune response. This, in turn, leads to overgrowth of superinfecting bacteria and yeast [90, 91, 92, 93]. The development of antimicrobial resistance will escalate peri-implant disease in the coming years. Therefore, the need for microbial sampling and testing is mandatory in order to prevent the risk of superinfection. These tests will identify the presence of ongoing specific microbial challenges that are difficult to eliminate and allow disease to progress. Moreover, strict supportive maintenance therapy should be considered to prevent disease recurrence and to keep ecological balance in the oral microbiota [94]. Therefore, the presence of antimicrobial agents that do not alter colonization resistance will lead to a decrease in the risk of development, spread and dissemination of resistant strains among patients [91].


6. Conclusion and future perspectives

Peri-implantitis is heterogeneous, polymicrobial infection where certain core microbiota may pose a significant role. Scientific evidence identifying the specific microbiota responsible for the development and progression of peri-implant infection is still inconclusive. A review of the literature points to an enrichment of well-recognized pathogens in addition to newly proposed pathogenic microorganisms, several of which have not yet been cultivated. Therefore, understanding the peri-implantitis microbiota will improve strategies for prevention, supportive therapy, risk assessment, early diagnosis of peri-implantitis, and timely intervention—all key aspects of long-term survival of dental implants [95]. Based on the available knowledge presented in the literature, Figure 1 summarizes important tips to the clinician. Future studies designed to understand the peri-implantitis microbiota should include careful selection of cases and controls, and the incorporation of state-of-the-art approaches, such as metagenomics [95].

Figure 1.

Tips for the clinician regarding peri-implantitis.


  1. 1. Albrektsson T, Dahlin C, Jemt T, Sennerby L, Turri A, Wennerberg A. Is marginal bone loss around oral implants the result of a provoked foreign body reaction? Clinical Implant Dentistry and Related Research. 2014;16(2):155-165
  2. 2. Lindhe J, Meyle J, Group DoEWoP. Peri-implant diseases: Consensus report of the sixth European workshop on periodontology. Journal of Clinical Periodontology. 2008;35(8 Suppl):282-285
  3. 3. Charalampakis G. Peri-Implantitis from a Microbiological Perspective. 2013
  4. 4. Boucher CO. Current Clinical Dental Terminology, a Glossary of Accepted Terms in all Disciplines of Dentistry. St. Louis: Mosby; 1963
  5. 5. Jermyn AC. Peri-implantoclaisa: Cause and treatment. International Journal of Implant Dentistry. 1958;5:25-48
  6. 6. Mombelli A, Oosten M, Schürch E, Lang N. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiology and Immunology. 1987;2(4):145-151
  7. 7. Levignac J. Periimplantation osteolysis- periimplantosis - periimplantitis. [Article in French]. Revue Française d'Odonto-Stomatologie 1965;8:1251-1260
  8. 8. Mombelli A, van Oosten MAC, Schürch E, Lang NP. The microbiota associated with successful or failing osseointegrated titanium implants. Oral Microbiology and Immunology. 1987;2(4):145-151
  9. 9. Tonetti M. Peri-implantitis: Biological considerations. Journal de Parodontologie. 1996;15:269-284
  10. 10. Tomasi C, Derks J. Clinical research of peri-implant diseases--quality of reporting, case definitions and methods to study incidence, prevalence and risk factors of peri-implant diseases. Journal of Clinical Periodontology. 2012;39(12 Suppl):207-223
  11. 11. Mombelli A, Muller N, Cionca N. The epidemiology of peri-implantitis. Clinical Oral Implants Research. 2012;23(Suppl 6):67-76
  12. 12. Zarb GAAT. Consensus report: Towards optimized treatment outcomes for dental implants. The Journal of Prosthetic Dentistry. 1998;80(6):641
  13. 13. Zitzmann NU, Berglundh T. Definition and prevalence of peri-implant diseases. Journal of Clinical Periodontology. 2008;35(8 Suppl):286-291
  14. 14. Lang NP, Berglundh T. Periimplant diseases: Where are we now?--consensus of the seventh European workshop on periodontology. Journal of Clinical Periodontology. 2011;11:178-181
  15. 15. Becker ST, Beck-Broichsitter BE, Graetz C, Dorfer CE, Wiltfang J, Hasler R. Peri-implantitis versus periodontitis: Functional differences indicated by transcriptome profiling. Clinical Implant Dentistry and Related Research. 2014;16(3):401-411
  16. 16. Heitz-Mayfield LJA, Lang NP. Comparative biology of chronic and aggressive periodontitis vs. peri-implantitis. Periodontology 2000. 2010;53(1):167-181
  17. 17. Karoussis IK, Salvi GE, Heitz-Mayfield LJA, Brägger U, Hämmerle CHF, 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. Clinical Oral Implants Research. 2003;14(3):329-339
  18. 18. 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. Journal of Clinical Periodontology. 2006;33(4):290-295
  19. 19. Heitz-Mayfield LJ. Peri-implant diseases: Diagnosis and risk indicators. Journal of Clinical Periodontology. 2008;35(8 Suppl):292-304
  20. 20. Berglundh T, Zitzmann NU, Donati M. Are peri-implantitis lesions different from periodontitis lesions?, Journal of Clinical Periodontology. 2011;38(11 Suppl):188-202
  21. 21. Wong RL, Hiyari S, Yaghsezian A, Davar M, Lin YL, Galvan M, et al. Comparing the healing potential of late-stage periodontitis and Peri-Implantitis. The Journal of Oral Implantology. 2017;43(6):437-445
  22. 22. Maruyama N, Maruyama F, Takeuchi Y, Aikawa C, Izumi Y, Nakagawa I. Intraindividual variation in core microbiota in peri-implantitis and periodontitis. Scientific Reports. 2014;4:6602
  23. 23. Zitzmann NU, Berglundh T, Ericsson I, Lindhe J. Spontaneous progression of experimentally induced periimplantitis. Journal of Clinical Periodontology. 2004;31(10):845-849
  24. 24. Charalampakis G, Abrahamsson I, Carcuac O, Dahlen G, Berglundh T. Microbiota in experimental periodontitis and peri-implantitis in dogs. Clinical Oral Implants Research. 2013
  25. 25. Marsh PD. Microbial ecology of dental plaque and its significance in health and disease. Advances in Dental Research. 1994;8(2):263-271
  26. 26. Marsh PD. Are dental diseases examples of ecological catastrophes? Microbiology. 2003;149(2):279-294
  27. 27. Heuer W, Elter C, Demling A, Neumann A, Suerbaum S, Hannig M, Heidenblut T, Bach FW, Stiesch‐Scholz M. Analysis of early biofilm formation on oral implants in man. Journal of Oral Rehabilitation 2007;34(5):377-82
  28. 28. Quirynen M, Vogels R, Pauwels M, Haffajee AD, Socransky SS, Uzel NG, et al. Initial subgingival colonization of ‘pristine’ pockets. Journal of Dental Research. 2005;84(4):340-344
  29. 29. WA J, GR J, Claudia B, Tiddo F. Early colonization of dental implants by putative periodontal pathogens in partially edentulous patients. Clinical Oral Implants Research. 2000;11(6):511-520
  30. 30. Griffen AL, Beall CJ, Firestone ND, Gross EL, DiFranco JM, Hardman JH, et al. CORE: A Phylogenetically-curated 16S rDNA database of the Core oral microbiome. PLoS One. 2011;6(4):e19051
  31. 31. Costalonga M, Herzberg MC. The oral microbiome and the immunobiology of periodontal disease and caries. Immunology Letters. 2014;162(2 0 0):22-38
  32. 32. Zaura E, Keijser BJF, Huse SM, Crielaard W. Defining the healthy “core microbiome” of oral microbial communities. BMC Microbiology. 2009;9:259
  33. 33. Valente NA, Andreana S. Peri-implant disease: What we know and what we need to know. Journal of Periodontal & Implant Science. 2016;46(3):136-151
  34. 34. Apse P, Ellen RP, Overall CM, Zarb GA. 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. 1989;24(2):96-105
  35. 35. Leonhardt A, Adolfsson B, Lekholm U, Wikstrom M, Dahlen G. A longitudinal microbiological study on osseointegrated titanium implants in partially edentulous patients. Clinical Oral Implants Research. 1993;4(3):113-120
  36. 36. Quiryen M, Listgarten MA. The distribution of bacterial morphotypes around natural teeth and titanium implants ad modum Brånemark. Clinical Oral Implants Research. 1990;1(1):8-12
  37. 37. Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. Journal of Clinical Periodontology. 2011;38(11 Suppl):203-213
  38. 38. Carcuac O, Derks J, Charalampakis G, Abrahamsson I, Wennstrom J, Berglundh T. Adjunctive systemic and local antimicrobial therapy in the surgical treatment of Peri-implantitis: A randomized controlled clinical trial. Journal of Dental Research. 2015
  39. 39. Charalampakis G, Belibasakis GN. Microbiome of peri-implant infections: Lessons from conventional, molecular and metagenomic analyses. Virulence. 2015;6(3):183-187
  40. 40. Dabdoub SM, Tsigarida AA, Kumar PS. Patient-specific analysis of periodontal and Peri-implant microbiomes. Journal of Dental Research. 2013;92(12_suppl):168S-175S
  41. 41. Kumar PS, Mason MR, Brooker MR, O'Brien K. Pyrosequencing reveals unique microbial signatures associated with healthy and failing dental implants. Journal of Clinical Periodontology. 2012;39(5):425-433
  42. 42. Griffen AL, Beall CJ, Campbell JH, Firestone ND, Kumar PS, Yang ZK, et al. Distinct and complex bacterial profiles in human periodontitis and health revealed by 16S pyrosequencing. The Isme Journal. 2011;6:1176
  43. 43. Abusleme L, Dupuy AK, Dutzan N, Silva N, Burleson JA, Strausbaugh LD, et al. The subgingival microbiome in health and periodontitis and its relationship with community biomass and inflammation. The Isme Journal. 2013;7:1016
  44. 44. Lafaurie GI, Sabogal MA, Castillo DM, Rincon MV, Gomez LA, Lesmes YA, et al. Microbiome and microbial biofilm profiles of Peri-Implantitis: A systematic review. Journal of Periodontology. 2017;88(10):1066-1089
  45. 45. Padial-Molina M, López-Martínez J, O’Valle F, Galindo-Moreno P. Microbial Profiles and Detection techniques in Peri-implant diseases: A systematic review. Journal of Oral & Maxillofacial Research. 2016;7(3):e10
  46. 46. Leonhardt Å, Renvert S, Dahlén G. Microbial findings at failing implants. Clinical Oral Implants Research. 1999;10(5):339-345
  47. 47. Albertini M, López-Cerero L, O'Sullivan MG, Chereguini CF, Ballesta S, Ríos V, et al. Assessment of periodontal and opportunistic flora in patients with peri-implantitis. Clinical Oral Implants Research. 2015;26(8):937-941
  48. 48. Botero JE, González AM, Mercado RA, Olave G, Contreras A. Subgingival microbiota in Peri-implant mucosa lesions and adjacent teeth in partially edentulous patients. Journal of Periodontology. 2005;76(9):1490-1495
  49. 49. Salvi GE, Fürst MM, Lang NP, Persson GR. One-year bacterial colonization patterns of Staphylococcus aureus and other bacteria at implants and adjacent teeth. Clinical Oral Implants Research. 2008;19(3):242-248
  50. 50. Fürst MM, Salvi GE, Lang NP, Persson GR. Bacterial colonization immediately after installation on oral titanium implants. Clinical Oral Implants Research. 2007;18(4):501-508
  51. 51. Al-Radha ASD, Pal A, Pettemerides AP, Jenkinson HF. Molecular analysis of microbiota associated with peri-implant diseases. Journal of Dentistry. 2012;40(11):989-998
  52. 52. Apatzidou D, Lappin DF, Hamilton G, Papadopoulos CA, Konstantinidis A, Riggio MP. Microbiome of peri-implantitis affected and healthy dental sites in patients with a history of chronic periodontitis. Archives of Oral Biology. 2017;83:145-152
  53. 53. Shibli JA, Melo L, Ferrari DS, Figueiredo LC, Faveri M, Feres M. Composition of supra- and subgingival biofilm of subjects with healthy and diseased implants. Clinical Oral Implants Research. 2008;19(10):975-982
  54. 54. Zheng H, Xu L, Wang Z, Li L, Zhang J, Zhang Q, et al. Subgingival microbiome in patients with healthy and ailing dental implants. Scientific Reports. 2015;5:10948
  55. 55. Koyanagi T, Sakamoto M, Takeuchi Y, Maruyama N, Ohkuma M, Izumi Y. Comprehensive microbiological findings in peri-implantitis and periodontitis. Journal of Clinical Periodontology. 2013;40(3):218-226
  56. 56. Tamura NOM, Miyakawa H, Nakazawa F. Analysis of bacterial flora associated with peri-implantitis using obligate anaerobic culture technique and 16S rDNA gene sequence. The International Journal of Oral & Maxillofacial Implants. 2013;28(6):1521-1529
  57. 57. da Silva ESC, Feres M, Figueiredo LC, Shibli JA, Ramiro FS, Faveri M. Microbiological diversity of peri-implantitis biofilm by sanger sequencing. Clinical Oral Implants Research. 2014;25(10):1192-1199
  58. 58. Ebadian AR, Kadkhodazadeh M, Zarnegarnia P, Dahlén G. Bacterial analysis of Peri-implantitis and chronic periodontitis in Iranian subjects. Acta Medica Iranica. 2012:7
  59. 59. Casado PL, Otazu IB, Balduino A, de Mello W, Barboza EP, Duarte MEL. Identification of periodontal pathogens in healthy Periimplant sites. Implant Dentistry. 2011;20(3):226-235
  60. 60. Canullo L, Peñarrocha-Oltra D, Covani U, Botticelli D, Serino G, Penarrocha M. Clinical and microbiological findings in patients with peri-implantitis: A cross-sectional study. Clinical Oral Implants Research. 2016;27(3):376-382
  61. 61. Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B. Microbiological findings and host response in patients with peri-implantitis. Clinical Oral Implants Research. 2002;13(4):349-358
  62. 62. Cortelli SC, Cortelli JR, Romeiro RL, Costa FO, Aquino DR, Orzechowski PR, et al. Frequency of periodontal pathogens in equivalent peri-implant and periodontal clinical statuses. Archives of Oral Biology. 2013;58(1):67-74
  63. 63. Ata-Ali J, Flichy-Fernández AJ, Alegre-Domingo T, Ata-Ali F, Palacio J, Peñarrocha-Diago M. Clinical, microbiological, and immunological aspects of healthy versus peri-implantitis tissue in full arch reconstruction patients: A prospective cross-sectional study. BMC Oral Health. 2015;15(1):43
  64. 64. Wang H-L, Garaicoa-Pazmino C, Collins A, Ong H-S, Chudri R, Giannobile WV. Protein biomarkers and microbial profiles in peri-implantitis. Clinical Oral Implants Research. 2016;27(9):1129-1136
  65. 65. Zhuang L-F, Watt RM, Mattheos N, Si M-S, Lai H-C, Lang NP. Periodontal and peri-implant microbiota in patients with healthy and inflamed periodontal and peri-implant tissues. Clinical Oral Implants Research. 2016;27(1):13-21
  66. 66. Eick S, Ramseier CA, Rothenberger K, Brägger U, Buser D, Salvi GE. Microbiota at teeth and implants in partially edentulous patients. A 10-year retrospective study. Clinical Oral Implants Research. 2016;27(2):218-225
  67. 67. Verdugo F, Castillo A, Simonian K, Russo P, D'Addona A, Raffaelli L, et al. Periodontopathogen and Epstein-Barr virus contamination affects transplanted bone volume in sinus augmentation. Journal of Periodontology. 2012;83(2):162-173
  68. 68. Canullo LPP, Botticelli D, Covani U, Jankovic S, Jovanovic T, Rakic M. What is the impact of Epstein-Barr virus in Peri-implant infection? The International Journal of Oral & Maxillofacial Implants. 2018;33(1):58-63
  69. 69. Belibasakis GN, Mir-Mari J, Sahrmann P, Sanz-Martin I, Schmidlin PR, Jung RE. Clinical association of Spirochaetes and Synergistetes with peri-implantitis. Clinical Oral Implants Research. 2016;27(6):656-661
  70. 70. Koyanagi T, Sakamoto M, Takeuchi Y, Ohkuma M, Izumi Y. Analysis of microbiota associated with peri-implantitis using 16S rRNA gene clone library. Journal of Oral Microbiology. 2010;2(1):5104
  71. 71. Yu X-L, Chan Y, Zhuang L-F, Lai H-C, Lang NP, Lacap-Bugler DC, et al. Distributions of Synergistetes in clinically-healthy and diseased periodontal and peri-implant niches. Microbial Pathogenesis. 2016;94:90-103
  72. 72. Al-Ahmad A, Muzafferiy F, Anderson AC, Wolber JP, Ratka-Kruger P, Fretwurst T, et al. Shift of microbial composition of peri-implantitis-associated oral biofilm as revealed by 16S rRNA gene cloning. Journal of Medical Microbiology. 2018;67(3):332-340
  73. 73. Tsigarida AA, Dabdoub SM, Nagaraja HN, Kumar PS. The influence of smoking on the Peri-implant microbiome. Journal of Dental Research. 2015;94(9):1202-1217
  74. 74. Group TNHW, Peterson J, Garges S, Giovanni M, McInnes P, Wang L, et al. The NIH human microbiome project. Genome Research. 2009;19(12):2317-2323
  75. 75. Frank JA, Reich CI, Sharma S, Weisbaum JS, Wilson BA, Olsen GJ. Critical evaluation of two primers commonly used for amplification of bacterial 16S rRNA genes. Applied and Environmental Microbiology. 2008;74(8):2461-2470
  76. 76. DeLong EF, Preston CM, Mincer T, Rich V, Hallam SJ, Frigaard N-U, et al. Community genomics among stratified microbial assemblages in the Ocean's interior. Science. 2006;311(5760):496-503
  77. 77. Streit WR, Schmitz RA. Metagenomics – The key to the uncultured microbes. Current Opinion in Microbiology. 2004;7(5):492-498
  78. 78. Rams TE, Degener JE, van Winkelhoff AJ. Antibiotic resistance in human peri-implantitis microbiota. Clinical Oral Implants Research. 2014;25(1):82-90
  79. 79. Verdugo F, Castillo A, Simonian K, Castillo F, Farez-Vidal E, D'Addona A. Periodontopathogen and Epstein–Barr virus-associated Periapical periodontitis may be the source of retrograde infectious Peri-Implantitis. Clinical Implant Dentistry and Related Research. 2015;17(1):199-207
  80. 80. Heitz-Mayfield LJ, Salvi GE, Mombelli A, Faddy M, Lang NP, Implant Complication Research G. Anti-infective surgical therapy of peri-implantitis. A 12-month prospective clinical study. Clinical Oral Implants Research. 2012;23(2):205-210
  81. 81. van Winkelhoff AJ, Wolf JW. Actinobacillus actinomycetemcomitans-associated peri-implantitis in an edentulous patient. A case report. Journal of Clinical Periodontology. 2000;27(7):531-535
  82. 82. Leonhardt A, Dahlen G, Renvert S. Five-year clinical, microbiological, and radiological outcome following treatment of peri-implantitis in man. Journal of Periodontology. 2003;74(10):1415-1422
  83. 83. Serino G, Turri A. Outcome of surgical treatment of peri-implantitis: Results from a 2-year prospective clinical study in humans. Clinical Oral Implants Research. 2011;22(11):1214-1220
  84. 84. Khoury F, Buchmann R. Surgical therapy of peri-implant disease: A 3-year follow-up study of cases treated with 3 different techniques of bone regeneration. Journal of Periodontology. 2001;72(11):1498-1508
  85. 85. Emrani J, Chee W, Slots J. Bacterial colonization of oral implants from nondental sources. Clinical Implant Dentistry and Related Research. 2009;11(2):106-112
  86. 86. Mombelli A, Lang NP. Antimicrobial treatment of peri-implant infections. Clinical Oral Implants Research. 1992;3(4):162-168
  87. 87. Roos-Jansåker A-M, Renvert H, Lindahl C, Renvert S. Surgical treatment of peri-implantitis using a bone substitute with or without a resorbable membrane: A prospective cohort study. Journal of Clinical Periodontology. 2007;34(7):625-632
  88. 88. Claffey N, Clarke E, Polyzois I, Renvert S. Surgical treatment of peri-implantitis. Journal of Clinical Periodontology. 2008;35(8 Suppl):316-332
  89. 89. Poveda Roda R, Bagán JV, Sanchis Bielsa JM, Carbonell Pastor E. Antibiotic Use in Dental Practice: A Review. Medicina Oral, Patología Oral Y Cirugía Bucal (Internet). 2007;12:186-192
  90. 90. Sullivan A, Edlund C, Nord CE. Effect of antimicrobial agents on the ecological balance of human microflora. The Lancet Infectious Diseases. 2001;1(2):101-114
  91. 91. Rashid MU, Weintraub A, Nord CE. Effect of new antimicrobial agents on the ecological balance of human microflora. Anaerobe. 2012;18(2):249-253
  92. 92. Nord CE. Studies on the ecological impact of antibiotics. European Journal of Clinical Microbiology & Infectious Diseases. 1990;9(7):517-518
  93. 93. Van der Waaij D, Nord CE. Development and persistence of multi-resistance to antibiotics in bacteria; an analysis and a new approach to this urgent problem. International Journal of Antimicrobial Agents. 2000;16(3):191-197
  94. 94. Verdugo F, Laksmana T, Uribarri A. Systemic antibiotics and the risk of superinfection in peri-implantitis. Archives of Oral Biology. 2016;64:39-50
  95. 95. Teles FRF. The microbiome of Peri-implantitis: Is it unique? The Compendium of Continuing Education in Dentistry. 2017;38:22-25

Written By

Dalia Khalil and Margareta Hultin

Submitted: 04 March 2018 Reviewed: 13 June 2018 Published: 05 November 2018