Resumen de Differences in Peri-Implant Microflora Between Fully and Partially Edentulous Patients: A Systematic Review
Background: The current evidence suggests that the oral microflora differs between individuals who are fully edentulous (FES) and those who are partially edentulous (PES). It is unknown whether this leads to differences in peri-implant microflora when implants are installed. The aim of the study is to compare the submucosal peri-implant microflora between FES and PES.
Methods: A systematic review was conducted. The MEDLINE, Embase, and Cochrane databases were searched for publications up to September 1, 2012. To reduce methodologic variations, only studies reporting in the same article about the submucosal peri-implant microflora of FES and PES were selected.
Results: Eleven publications describing 10 studies were selected. Because of numerous differences among the selected studies, no meta-analysis could be performed. Six of 10 studies showed a significant difference in the composition of the submucosal peri-implant microflora in healthy and peri-implant mucositis conditions between FES and PES, with the latter showing a potentially more pathogenic composition. However, microbiologic results were not unanimous among the studies.
Conclusions: In healthy and peri-implant mucositis conditions, PES harbor a potentially more pathogenic peri-implant microflora than FES. The current data are insufficient for a clear conclusion regarding peri-implantitis cases. Overall, because of the lack of a meta-analysis, the variability in microbiologic outcomes and the limited number of studies available, the current evidence seems not to be robust.
The oral cavity is the single site in the human body that provides non-shedding surfaces for microbial colonization. This and the oral environmental conditions facilitate growth of numerous microorganisms and development of dental biofilms.1 Disturbance of the balance between the oral microflora and the host immune response may result in infection and destructive inflammatory responses in the periodontal tissues. Research on microorganisms associated with periodontal disease has been extensive. Based on studies using predominately microscopy and cultural techniques, a number of species, including Aggregatibacter actinomycetemcomitans (Aa), Porphyromonas gingivalis (Pg), and Tannerella forsythia (Tf), have been associated with periodontitis.2,3 These species have also been associated most strongly with periodontal disease progression and unsuccessful periodontal therapy (for review, see Haffajee and Socransky2) and, as such, were designated as periodontal pathogens during the 1996 World Workshop of Periodontology.4 It has been suggested that these periodontal pathogens may also play a role in the development and progression of peri-implant mucositis and peri-implantitis. Several studies have shown distinct differences between the microflora associated with healthy and inflamed peri-implant tissues.5-7 In these studies, Aa, Fusobacterium nucleatum (Fn), Pg, Prevotella intermedia (Pi), and Tf were detected more frequently around unsuccessful implants than in healthy implant sites. However, the use of new analyzing techniques, such as polymerase chain reaction (PCR) and pyrosequencing, has revealed that the periodontal and peri-implant microflora are far more diverse than previously thought and may harbor �uncultivable� species of which the potential pathogenic role in periodontal and peri-implant diseases is unknown.8,9 It has been suggested that elimination of the subgingival environment by extraction of all teeth reduces the number of periodontal pathogens present in the oral cavity. Extraction of partially erupted third molars has been found to significantly reduce the detection frequency of black-pigmented Gram-negative bacteria and Aa.10 Danser et al.11 could no longer culture Aa and Pg from oral mucosal sites after extraction of all natural teeth in individuals initially culture-positive for these microorganisms. This observation suggested that the periodontal sulcus may be the primary habitat of these periodontal species. This was in line with the notion that both pathogens were not detected from peri-implantitis lesions in individuals who are fully edentulous (FES).5 A more recent study, applying real-time PCR technology, showed that full-mouth tooth extraction does not result in eradication but merely in a significant reduction of these periodontal pathogens.12 This finding is supported by various cross-sectional studies showing that Aa and Pg can be detected in the oral cavity of FES.13-17 A comparison between the microflora on removable full dentures in FES and the supragingival plaque from periodontally healthy individuals and chronic periodontitis patients revealed marked differences between the groups in both the �hard-surface� samples and the soft-tissue and saliva samples.17 It was suggested that the nature of the hard-tissue surface influences the composition of the biofilm and that gingival sulcus fluid might be essential for the colonization of some bacterial species.
Placement of dental implants in the edentulous oral cavity establishes a submucosal subgingival-like environment. Several studies have investigated the effect of implant placement on the microflora of the edentulous oral cavity, but contradicting results have been reported.18-20 Using the checkerboard DNA�DNA hybridization technique, Lee et al.18 found no differences in the composition of the tongue microbiota before and after implant placement and between tongue and peri-implant microflora after implant placement. Devides and Franco19 evaluated the presence of three periodontal pathogens in the mandibular arch of FES before and after implant placement by analyzing samples obtained from the alveolar ridge and peri-implant sulcus using PCR. Higher detection frequencies of Aa and Pg were observed after implant placement and with an increasing detection rate the longer the implants were in function, whereas no differences were observed for Pi. Quirynen and Van Assche20 evaluated the oral microflora from full-mouth tooth extraction, during 9 months of full edentulism, up to 1 year after abutment connection. Full-mouth tooth extraction resulted in reduction of the total aerobic and anaerobic bacterial load (culture), and levels remained stable after subsequent implant placement. Using both quantitive PCR (qPCR) and the checkerboard technique, no differences were observed in detection frequency of key periodontal pathogens at the different time intervals. However, significantly higher total numbers of Pg, Tf, and Pi, but not for Aa, were observed in teeth, saliva, and tongue samples that were taken before full-mouth extraction compared to the edentulous and postimplantation situation.
The proportions of different bacterial species have been found to differ markedly on different intraoral surfaces.21 Using the checkerboard technique to analyze 40 different species, it was concluded that the microflora of the different soft-tissue sites differs from the microflora that colonizes the supragingival and subgingival locations at teeth. In FES, the microorganisms colonizing implants originate primarily from the intraoral soft tissues, whereas in individuals who are partially edentulous (PES), the subgingival area of neighboring teeth can also be a principal source. Great similarities in the composition of the subgingival microflora at implants and teeth within the same mouth have been found.22-26 In fact, after implant placement, a similar subgingival microflora can be found at implants and teeth after just a few days.27-29 A systematic review comparing long-term clinical performance of dental implants in FES and PES showed that FES generally harbor more plaque at their implants than PES.30 However, no differences could be observed regarding probing depth (PD) and survival rate, whereas data regarding peri-implant mucosal bleeding were inconsistent. Apparently, the higher plaque levels observed in FES do not lead to impaired peri-implant conditions when compared with PES. From this, it might be hypothesized that not the quantity but rather the quality of the plaque, i.e., the microbial composition, plays a predominant role in the development of peri-implant infection. Whether a difference exists in the peri-implant microflora of FES and PES in health and/or disease is unknown at a systematic review level. Therefore, the aim of this study is to evaluate the peri-implant microflora in FES and PES by means of a systematic review.
