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Adhesion of microorganisms and maturation of implant dental plaque

As the processes involved in biofilm formation on implants are not significantly different from the processes involved in the formation of biofilms on natural teeth, this review focuses on fundamental principles and peculiarities in biofilms on dental implants.

With regard to the initial adherence of microorganisms to oral surfaces, early- colonizing bacteria have been identified, which interact directly with constituents of the acquired salivary pellicle. These early colonizers include Streptococcus and Actinomyces species, which prepare favorable conditions for the subsequent adherence of characteristic late-colonizers. Late-colonizing bacteria include microorganisms that are associated with diseases such as caries or periodontitis, representing a shift toward an increased pathogenic character of dental plaque within days (Ramberg et al., 2003; Furst et al., 2007). Regarding the similarities observed between periodontal and periimplant inflammatory processes, several bacteria have been associated with inflammatory periodontal processes, and periodontal research has highlighted that subgingival plaque is organized in five characteristic complexes. One of these complexes (“red complex”)—including Tannerella forsythia, Porphyromonas gin- givalis, and Treponema denticula—is particularly related to clinical symptoms of periodontal disease, while others—including Streptococcus species, Veillonella par- vula, and Actinomyces odontolyticus—are rather associated with periodontal health (Socransky et al., 1998). In addition, other bacteria that are not regularly associated with Socransky’s complexes, such as Aggregatibacter actinomycetemcomitans, Prevotella intermedia, Parvimonas micra, Fusobacterium nucleatum, and Eubacterium nodatum, have been related to periodontal inflammation, too (Perez-Chaparro et al., 2014). However, although studies until 2015 have highlighted that the microbiota associated with periodontal inflammation is by far more complex than previously assumed (Hajishen- gallis, 2015), microbial analysis of biofilm constituents in dental implants have concentrated on the pathogens putatively associated with periodontitis, hypothesizing that these microorganisms do also play an essential role in the pathogenesis of periimplant infections and inflammatory processes.

Due to the narrow entrance of periimplant pockets, it is difficult to harvest biofilms adherent to the implant surface; thus, in very most investigations, sterile paper points were placed in the periimplant pockets for gathering samples of subgingival implant plaque. However, this procedure involves an overrepresentation of loosely adhered or planktonic microorganisms in the samples, which features the disadvantage that not only microorganisms organized in the biofilm adherent to the implant surface are subject to analysis (Quirynen et al., 2006). For analyzing the microbial composition in the subgingival plaque samples, various techniques including conventional methods such as culturing and molecular methods, such as (real-time) polymerase chain reaction (PCR) and checkerboard DNA-DNA hybridization, have been employed in the vast majority of studies; the latter techniques have the disadvantage that due to the necessity of targeted primers and probes only prior selected microorganisms can be identified (Charalampakis and Belibasakis, 2015). As a result of these restrictions and narrowed by the hypothesis that periimplant infections are caused by the same microbial pathogens as periodontal infections, the focus of very most studies was set on identifying periodontal pathogens on implant surfaces. In successfully osseointe- grated implants, the microflora identified was dominated by Streptococcus species such as Streptococcus intermedius, Streptococcus oralis, Streptococcus sanguinis, Streptococcus gordonii, V parvula, F. nucleatum, and Capnocytophaga gingivalis (Lee et al., 1999). However, although similar processes are involved in biofilm formation on teeth and implant surfaces, numerous researchers have highlighted substantial differences in the microbiota organized in biofilms on teeth and implants. Many studies demonstrated that microbial colonization of implants occurs very quickly after completion of surgery (De Boever and De Boever, 2006; Quirynen et al., 2006; Furst et al., 2007). However, conflicting data regarding the microbial species involved in the formation of biofilms on the surface of implants and teeth during the initial phases of biofilm formation have been published, as either similar (Quirynen et al., 2006) or distinct patterns (De Boever and De Boever, 2006; Furst et al., 2007) have been observed. With regard to this aspect, it has been highlighted that the dental status significantly impacts microbial colonization of implant surfaces, as in partially edentulous patients, microorganisms from the subgingival areas of teeth may invade implant sites and lead to colonization of implant surfaces, suggesting that in edentulous patients without any subgingival reservoir no transition of periodontal pathogens occurs. The impact of periodontitis in partially edentulous patients on the initial adherence of bacteria to titanium implants has been addressed by a Mexican group only in 2016. The authors employed a supragingival approach to simulate biofilm formation on titanium specimens in subjects with periodontitis and in periodontally healthy subjects for 48 h and identified significantly higher levels of Treponema denticola, Neisseria mucosa, Eikenella corrodens, and T. forsythia in subjects with periodontitis, while in periodontally healthy subjects significantly higher levels of Capnocytophaga sputigena, Fusobacterium periodonticum, Prevotella melaninogenica, and Streptococcus mitis were discovered (Martinez-Hernandez et al., 2016). This observation is particularly interesting as meta-analyses have highlighted a significantly higher odds ratio for implant success in patients without than in patients with a history of periodontitis (Safii et al., 2010).

Regarding the shift toward a pathogenic character of implant plaque with time, a meta-analysis has been performed by Mombelli and Decaillet in 2011 to summarize the scientific evidence available for the properties of biofilms in periimplant diseases. The authors identified similarities in the microflora of biofilms in subjects with periodontitis and periimplant infections, suggesting that in many cases, microorganisms that are ubiquitous in subjects with chronic periodontitis such as Fusobacterium species and P. intermedia are frequently also identified in subjects with periimplant infections. In addition, microorganisms, such as A. actinomycetemcomitans, which are not commonly identified in periodontal infections, are not regularly associated with periimplant infections, too (Mombelli and Decaillet, 2011).

Some microorganisms, such as Staphylococcus aureus, P. intermedia, and P. gin- givalis, have been associated with high affinity toward titanium surfaces (Harris and Richard, 2004; Kuula et al., 2004). However, conflicting data regarding the presence of S. aureus in the oral cavity have been published, as it has been identified on both teeth and implants and only its presence on teeth was predictive of being also present on implants (Renvert et al., 2008). Other researchers identified S. aureus as a member of the transient flora of the oral cavity regardless of periodontal conditions (Koukos et al., 2015). In addition to that, some researchers have attributed S. aureus a crucial role in the etiology of periimplant inflammatory processes and implant failure (Kronstrom et al., 2001), while other researchers failed to establish a correlation (Charalampakis et al., 2012; Zhuang et al., 2016).

The latest studies investigating microbial biofilms on dental implant surfaces employed metagenomic analyses to overcome the restrictions associated with the use of molecular analyses. However, Charalampakis and Belibasakis (2015) highlighted that it is possible that unfrequent microorganisms with different target sequences are not identified with this method, too, assuming that genes encoding virulence factors can only be found in a subset of microbial strains. Thus, the few studies that employed a metagenomic approach for investigating biofilms in subjects with periimplant infections have also to be interpreted with caution. Nevertheless, it was only recently observed that in partially edentulous patients with both periodontal and periimplant health and disease, 60% of the individuals included shared less than 50% of the species between their periodontal and periimplant biofilms, and 85% shared less than 8% of abundant species between tooth and implant biofilms. Moreover, in individuals where bacteria belonging to Socransky’s red complex were identified in the subgingival areas of teeth, they were identified in merely 37% of the periimplant sulci, too (Dabdoub et al., 2013). Similar results were reported by other groups, who employed a metagenomic approach for identifying differences in the overall bacterial composition of biofilms adherent to tooth and dental implant surfaces and identified a more complex microbial composition in implant biofilms; however, the overall prevalence of periodontal pathogens was low, yet higher in biofilms on implants than on teeth (Koyanagi et al., 2013). In contrast to these findings, other researchers maintain that the microbial flora in biofilms from sites with periimplant infections is less complex than in biofilms from tooth sites with and without periodontitis as well as from healthy implants; regarding the Gram-status, biofilms from implants harbour significantly higher levels of Gram-negative bacteria than biofilms from tooth sites (Kumar et al., 2012). For healthy implants and implants with periimplantitis, metagenomic analyses carried out in 2014 have identified higher levels of Actinomyces, Atopobium, Gemella, Kingella, Rothia, and Veillonella species and lower levels of Campylobacter, Desulfobulbus, Dialister, Eubacterium, Filifactor, Mitsukella, Porpyhromonas, and Pseudoramibacter species than in periimplant sites. In periimplant sites, higher proportions of bacterial species associated in Socransky’s orange complex such as

F. nucleatum, P. micra, P. intermedia, and Catonella gracilis, as well as several uncommon species including Dialister invisus, Streptococcus sp. human oral taxon (HOT) 064, Filifactor alocis, and Mitsuokella sp. HOT 131 were identified than in healthy implants (Da Silva et al., 2014).

These partially conflicting observations from the vast number of studies investigating biofilm formation on dental implant surfaces underline that—to date—the knowledge on biofilms in implant surfaces is still limited and highlight that biofilms on implant and tooth surfaces should be treated as distinct and separate ecosystems. Nevertheless, the existing data indicate that biofilms on implants harbor complex microbial communities. As bacteria involved in the pathogenesis of periodontal diseases are not necessarily involved in the pathogenesis of periimplant infections, further studies are necessary to elucidate the microbial mechanisms responsible for the onset and progress of periimplant infections.

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