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. 2022 Jun 16;10(6):1232. doi: 10.3390/microorganisms10061232

Table 1.

Studies included in this review and the main bacterial species identified in each study.

Article Title Authors Year of Publication Study Design Study Samples Population Characteristics Bacterial Isolation Technique Isolated Bacteria
Diversity analysis of subgingival microbial bacteria in periimplantitis in Uygur population Gao et al. [9] 2018 Observational Study 40 samples of gingival crevicular fluid divided into two groups: healthy implants (Control group) and periimplantitis (Case group) Uygur patients who had treatment with dental implants from 2013 to 2016 DNA extraction, PCR amplification and 16S rRNA gene sequencing Prevotella, Streptococcus, Acinetobacter, Fusobacterium, Neisseria, Porphyromonas, Treponema, Leptothrix, Capnocytophaga
Efficiency of photodynamic therapy in the treatment of periimplantitis—A three-month randomized controlled clinical trial Rakašević et al. [19] 2016 Randomized controlled clinical trial Samples from 52 periimplantitis sites divided into two groups (Study group and Control group) Patients with periimplantitis who presented in two dental clinics in Belgrade between January 2014 until February 2015 Bacterial culture for the diagnosis of aerobic and anaerobic pathogens Veillonella spp., Prevotella intermedia, Peptostreptococcus spp., Peptostreptococcus asaccharolyticus, Porphyromonas gingivalis, Fusobacterium nucleatum, Actinomyces odontolyticus
Bacterial profiles and proteolytic activity in periimplantitis versus healthy sites Neilands et al. [20] 2015 Non-randomized, controlled, clinical study 50 samples (25 from healthy subjects, 25 from periimplantitis sites) Patients with dental implants treatment in the past, attending maintenance appointments in a dental clinic in Sweden Bacterial culture on Brucella agar Porphyromonas/Prevotella, Fusobacterium, Tannerella, Streptococcus oralis, Streptococcus mitis, Streptococcus anginosus, Streptococcus constellatus, Streptococcus intermedius
Short-term effects of hyaluronic acid on the subgingival microbiome in periimplantitis: A randomized controlled clinical trial Soriano-Lerma et al. [21] 2020 Randomized controlled trial 108 samples divided into 3 groups (Test group, Control group 1, Control group 2) Patients diagnosticated with periimplantitis in a private dental office in Spain DNA isolation, PCR amplification and 16S rRNA gene sequencing Fusobacterium, Prevotella, Porphyromonas, Ralstonia, Sphingomonas, Streptococcus, Treponema, Propionibacterium, Alloprevotella, Veillonella, Lactobacillus, Haemophilus, Staphylococcus, Campylobacter, Tannerella
A randomized clinical trial of an adjunct diode laser application for the nonsurgical treatment of periimplantitis Arısan et al. [22] 2015 Randomized clinical trial Samples collected from 24 implants affected by periimplantitis at baseline and 1 month after intervention 10 patients diagnosticated with periimplantitis who went to the department clinic in Istanbul University between February 2010 and May 2013 DNA extraction, PCR amplification and hybridization procedures Actinomyces odontolyticus, Actinomyces viscosus, Aggregatibacteractinomycetemcomitans, Campylobacter concisus, Campylobacter gracilis, Campylobacterrectus/showae, Capnocytophaga gingivalis/sputigena/ochracea, Eikenella corrodens, Eubacterium nodatum, Fusobacterium nucleatum, Peptostreptococcus micros, Porphyromonas gingivalis, Prevotella intermedia, Prevotellanigrescens, Streptococcus constellatus group, Streptococcusgordonii group, Streptococcus mitis group, Tannerella forsythia (Bacteroides forsythus; Tannerella forsythensis), Treponema denticola, and Veillonella parvula.
The effects of Lactobacillus reuteri probiotics combined with azithromycin on periimplantitis: A randomized placebo-controlled study Tada et al. [23] 2017 Randomized placebo-controlled study Samples collected from periimplantitis sites at baseline and 4, 12, and 24 weeks after allocated treatment 30 patients diagnosticated with periimplantitis from 7 different institutions including Kyushu Dental University Hospital, Japan, divided into 2 groups, placebo and probiotics DNA isolation, PCR amplification and 16S rRNA gene sequencing Treponema denticola, Fusobacterium nucleatum, Peptostreptococcus micros, Streptococcus constellatus, Prevotella nigrescens, Tannerella forsythia, Campylobacter gracilis. Prevotella intermedia, Campylobacter rectus, Porphyromonas gingivalis, Veillonella parvula, Streptococcus gordonii, Capnocytophaga, Streptococcus mitis
Effectiveness of enamel matrix derivative on the clinical and microbiological outcomes following surgical regenerativetreatment of periimplantitis. A randomized controlled trial Isehed et al. [24] 2016 Randomized controlled trial Samples collected from the deepest pocket of the each implant at baseline, 2 weeks, 3, 6, and 12 months after surgery treatment 29 patients diagnosticated with periimplantitis from a periodontology clinic in Sweden DNA extraction with Gen Elute Bacterial Geno-mic DNA kit (Sigma Aldrich, St. Louis, MO, USA), bacterial characterization by the HOMIM microarray Fusobacteria (cluster probe), Parvimonas micra, Porphyromonas sp., Eubacterium nodatum, Porphyromonas gingivalis, Ochrobactrum anthropi, Tannerella forsythia and Campylobacter concisus/Campylobacter rectus.
Adjunctive Systemic and Local Antimicrobial Therapy in the Surgical Treatment of Periimplantitis: A Randomized Controlled Clinical Trial Carcuac et al. [25] 2016 Randomized Controlled Clinical Trial Samples collected from periimplantitis sites at baseline, 3, 6 and 12 months after surgery 100 patients with severe periimplantitis who were referred to 2 clinics specialized in periodontics in Sweden Culture and checkerboard DNA-DNA hybridization analyses Fusobacterium nucleatum, Prevotella intermedia/Prevotella nigrescens, Campylobacter rectus, Porphyromonas gingivalis, Tannerella forsythia, Porphyromonas endodontalis, Parvimonas micra
Comparison of the effects of air-powder abrasion, chemical decontamination, or their combination in open-flap surface decontamination of implants failed for periimplantitis: an ex vivo study Pranno et al. [26] 2021 Single-blind, randomized, controlled, ex vivo study 80 samples collected from the retrieved implants 20 patients from Oral Surgery Unit University of Rome with minimum 4 implants affected by periimplantitis which need to be explanted Bacterial culture techniques: for aerobic bacteria—Columbia sheep blood agar plates and for anaerobic—Schaedler sheep blood agar Staphylococcus aureus, Streptococcus mitis/oralis, Staphylococcus epidermidis and Streptococcus salivarius. Enterococcus faecalis, Candida albicans, Pseudomonas aeruginosa and Neisseria flavescens
The Efficacy of a Diode Laser on Titanium Implants for the Reduction of Microorganisms That Cause Periimplantitis Wawrzyk et al. [27] 2021 Clinical study Samples collected from saliva, the surfaces of the crowns and dental implants components 3 patients with advanced periimplantitis Bacterial culture technique of anaerobic using Schaedler horse blood agar Staphylococcus aureus, Streptococcus constellatus, Streptococcus oralis, Streptococcus pneumoniae, Rothia mucilaginosa, and Rothia aeria, and the following Gram-negative bacteria: Haemophilus parainfluenzae, Klebsiella pneumoniae, Klebsiella oxytoca, and Veilonella parvula. Candida guilliermondii, Actinomyces odontolyticus
Investigation of antibiotic susceptibility of the bacterial isolates and local flora changes after complex therapy in chronic periodontitis and periimplantitis Ciobanu et al. [28] 2018 Clinical study Samples collected from sites with periimplantitis before and after therapy Patients diagnosticated with chronic periimplantitis Culture examination Capnocytophaga spp., Prevotella oralis, S. intermedius, S. gordonii, Veillonella spp.
Shift of microbial composition of periimplantitis-associated oral biofilm as revealed by 16S rRNA gene cloning Al-Ahmad et al. [29] 2018 Cross-sectional study Samples collected from the deepest sites of periimplantitis and from the periimplantar healthy sulcus 10 patients with at least one implant affected by periimplantitis and one healthy implant DNA extraction and PCR amplification of 16S rRNA genes Streptococcus spp., Prevotella spp., Fusobacterium spp., Eubacterium spp., Porphyromonas gingivalis, Treponema spp., Campylobacter spp., Filifactor alocis, Abitrophia defectiva, Alloprevotella tannarae, Neisseria spp., Parvimonas micra, Selenomonas spp., Capnocytophaga spp., Atopobium spp., Peptostreptococcus spp., Tannerella forsythia, Scadovia wiggisiae, Bacteroidetes bacterium, Eikenella Corodens, Fretibacterium fastidiosum, Johnsonella ignava, Synergistales bacterium, Dialister invisus, Raoultella sp.
Subgingival microbiome in patients with healthy and ailing dental implants Zheng et al. [30] 2015 Clinical study Samples collected from periimplantar sulcus and pockets 10 patients with healthy implants, 8 patients with perimucositis and 6 with periimplantitis Microbial DNA extraction, 16S rRNA gene library preparation, and pyrosequencing Leptotrichia hofstadii, Eubacterium infirmum, Kingella denitrificans, Actinomycescardiffensis, Eubacterium minutum, Treponema lecithinolyticum, and Gemella sanguinis were higher in PI sites Streptococcus, Leptotrichia, Actinomyces, Capnocytophaga, Prevotella, Fusobacterium, Neisseria
Microbiota in Gingival Crevicular Fluid Before and After Mechanical Debridement With Antimicrobial Photodynamic Therapy in Periimplantitis Wang et al. [31] 2022 Clinical study 61 samples collected from all the implants: before treatment and 7, 14, 30, 60 and 180 days after treatment 9 patients presented at Department of Stomatology in Beijing Hospital with 14 implants affected by periimplantitis Bacterial 16S rRNA was amplified and sequenced using an Illumina MiSeq platform Bacteroidetes, Proteobacteria, Firmicutes, Fusobacteria, Spirochaetes, Synergistetes, and Actinobacteria Prevotella, Neisseria, Fusobacterium, Porphyromonas, Treponema, Streptococcus, Haemophilus, Capnocytophaga, Leptotrichia, and Fretibacterium
Microbiological findings in early and late implant loss: an observational clinical case-controlled study Korsch et al. [32] 2021 Observational clinical case–control study Samples collected from implants affected by severe periimplantitis without any chance of preservation and from healthy implants as controls 48 patients with 53 implants were introduced in the study DNA extraction, PCR amplification and 16S rRNA gene sequencing Treponema sp., Streptococcus, Fretibacterium, Anaerovoracaceae uncl, Desulfobulbus sp., Pseudoramibacter alactolyticus, Dialister pneumosintes, Streptococcus sanguinis, Shewanella sp., Pantoea sp., Haemophilus sp., Haemophilus parainfluenzae, Pseudomonas sp., Lautropia mirabilis, Actinomyces naeslundii
Strong oral plaque microbiome signatures for dental implant diseases identified by strain-resolution metagenomics Ghensi et al. [33] 2020 Clinical study Samples collected from each implant and from contralateral healthy implant or tooth for every patient included in the study 80 patients enrolled in the study: 28 with healthy implants, 28 with mucositis and 24 with periimplantitis DNA extraction P. gingivalis, T. forsythia, Treponema denticola, P. endodontalis, F. fastidiosum, Filifactor alocis, Desulfobulbus spp., T. lecithinolyticum
Cluster of bacteria associated with periimplantitis Persson et al. [12] 2014 Retrospective clinical study Samples collected at one implant with periimplantitis in each of 166 patients and from 47 healthy implants 166 patients with periimplantitis and 47 patients with healthy dental implants Checkerboard DNA–DNA hybridization Actinomyces odontolyticus, A. actinomycetemcomitans (a), Campylobacter gracilis, Campylobacter rectus, Campylobacter showae, Helicobacter pylori, Haemophilus influenzae, Leptothrichia buccalis, P. intermedia, Propionybacterium acnes, Porphyromonas endodontalis, P. gingivalis, Staph. aureus, Staph. anaerobius, Streptococcus intermedius, Streptococcus mitis, T. forsythia, T. denticola, and Treponema socranskii.
Microbiological diversity of periimplantitis biofilm by Sanger sequencing da Silva et al. [34] 2014 Clinical study Samples collected from the deepest pocket depth in the test group and from mesial site of healthy implants 20 individuals, 10 with healthy implants and 10 with at least one implant with periimplantitis, both groups with minimum 10 periodontally healthy teeth Extraction of DNA, PCR amplification of universal 16S rRNA Fusobacterium nucleatum, Campylobacter gracilis, Dialister invisus, Streptococcus sp., Eubacterium infirmum, Filifactor alocis and Mitsuokella sp., Parvimonas micra and Prevotella intermedia
Analysis of bacterial flora associated with periimplantitis using obligate anaerobic culture technique and 16S rDNA gene sequence Tamura et al. [35] 2013 Clinical study Samples collected from the deepest sites of the both groups, test and control 30 patients, 15 diagnosticated with periimplantitis, 15 with healthy implants Culture technique and 16S rDNA gene sequence Streptococcus, Eubacterium, Prevotella, Actinomyces, Fusobacterium, Eubacterium nodatum, Prevotella intermedia, Fusobacterium nucleatum, Filifactor alocis, E brachy, Parascardovia denticolenns, Parvimonas micra
Microbial profiles of peri-implant mucositis and periimplantitis: submucosal microbial dysbiosis correlates with disease severity Shi et al. [36] 2022 Cross-sectional study Samples collected from 64 patients, 27 with perimucositis and 37 with periimplantitis Patients with periimplantitis or perimucositis presented in Dep. Of Oral Implantology in Zhejiang University School of Medicine, China DNA extraction, PCR amplification and 16S rRNA gene sequencing Porphyromonas, Fusobacterium, Treponema and Prevotella, Campylobacter, Filifactor, Alloprevotella
Exploring the microbiome of healthy and diseased peri-implant sites using Illumina sequencing Sanz-Martin et al. [37] 2017 Clinical study Sample collection from 32 healthy implants and from 35 implants affected by periimplantitis Patients with healthy implants and with periimplantitis presented in center of Dental Medicine at the University of Zürich Bacterial nucleic acids isolation, sample DNA analyzed by sequencing the 16S rRNA gene V3-V4 hypervariable region Porphyromonas (phylum Bacteroidetes), Treponema (phylum Spirochetes), Filifactor (phylum Firmicutes), Fretibacterium (phylum Synergistetes) and Tannerella (phylum Bacteroidetes)
Intra-oral single-site comparisons of periodontal and peri-implant microbiota in health and disease Yu et al. [38] 2019 Clinical study Samples collected from 4 sites for each patient: Healthy implant, healthy tooth, periimplantitis site and periodontitis site 18 Chinese partial dentate patients with both periimplantitis and periodontitis DNA extraction, PCR amplification Bacteroidetes and Prevotella taxa (including P. denticola, P. multiformis and P. fusca).
Identification of microbiota in periimplantitis pockets by matrix assisted laser desorption/ionization time-of-flight mass spectrometry Yeh et al. [39] 2019 Clinical study Samples collected from periimplantitis pockets 12 patients with periimplantitis Culture examination Neisseria flavescen, Streptococcus constellatus, Slackia exigua, Streptococcus intermedius, Fusobacteriumnucleatum, Gemella morbillorum and Gram-positive anaerobic Bacillus
Intraindividual variation in core microbiota in periimplantitis and periodontitis Maruyama et al. [40] 2014 Clinical study Samples collected from the deepest pockets in periimplantitis sites and in periodontitis sites 20 Patients with both periimplantitis and periodontitis DNA extraction and PCR amplification of 16S rRNA genes Olsenella, Sphingomonas, Peptostreptococcus, unclassified Neisseriaceae, genus Desulfomicrobium, Actinomyces johnsonii, Fusobacterium nucleatum, Porphyromonas gingivalis, Streptococcus oralis, Treponema denticola, and Treponema socranskii Achromobacter xylosoxidans, Actinomyces massiliensis, and Porphyromonas sp.
The severity of human periimplantitislesions correlates with the level of submucosal microbial dysbiosis Kröger et al. [41] 2018 Cohort study or case–control study Samples collected from all 45 implants affected by periimplantitis 30 patients with at list one implant with periimplantitis DNA extraction and PCR amplification of 16S rRNA genes Eubacteriaceae, Fretibacterium sp., Fretibacterium fastidiosum, Peptostreptococcaceae, Alloprevotella sp., Fastidiosipila sanguinis, Filifactor alocis, Peptostreptococcaceae, Bacteriodetes bacterium, Treponema parvum, Clostridiales bacterium, and Orobacterium, Granulicatella elegans, Rothia aeria, Corynebacterium durum, Veillonella dispar, Acinetobacter