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Published in: International Journal of Implant Dentistry 1/2015

Open Access 01-12-2015 | Research

Real-time PCR analysis of fungal organisms and bacterial species at peri-implantitis sites

Authors: Frank Schwarz, Kathrin Becker, Sebastian Rahn, Andrea Hegewald, Klaus Pfeffer, Birgit Henrich

Published in: International Journal of Implant Dentistry | Issue 1/2015

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Abstract

Background

The potential role of fungal organisms and their co-aggregation with either periodontopathogens or opportunistic pathogens at peri-implantitis sites is unknown. The aim of the present study was to qualitatively/quantitatively analyze and correlate fungal organisms and bacterial species at peri-implantitis sites.

Methods

In a total of 29 patients, submucosal/subgingival plaque samples were collected at peri-implantitis and healthy implant sites as well as teeth with a history of periodontitis (controls). A real-time PCR assay was established for the qualification of fungal organisms and a TaqMan assay for the quantification of Porphyromonas gingivalis, Parvimonas micra, Tannerella forsythia, Mycoplasma salivarium, Veillonella parvula, and Staphylococcus aureus.

Results

Fungal organisms were more frequently identified at peri-implantitis (31.6%) (i.e., Candida albicans, Candida boidinii, Penicillium spp., Rhodotorula laryngis, Paelicomyces spp., Saccharomycetes, Cladosporium cladosporioides) and healthy implant sites (40% - Candida dubliniensis, C. cladosporioides) than at selected teeth (20% - C. albicans, Fusarium solani). At implant sites, fungal organisms were significantly correlated with P. micra and T. forsythia.

Conclusions

Candida spp. and other fungal organisms were frequently identified at peri-implantitis as well as healthy implant sites and co-colonized with P. micra and T. forsythia.
Literature
1.
go back to reference Lindhe J, Meyle J, Group DoEWoP. Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol. 2008;35:282–5.CrossRefPubMed Lindhe J, Meyle J, Group DoEWoP. Peri-implant diseases: consensus report of the sixth European workshop on periodontology. J Clin Periodontol. 2008;35:282–5.CrossRefPubMed
2.
go back to reference Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol. 2011;38 Suppl 11:203–13.CrossRefPubMed Mombelli A, Decaillet F. The characteristics of biofilms in peri-implant disease. J Clin Periodontol. 2011;38 Suppl 11:203–13.CrossRefPubMed
3.
go back to reference Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35:292–304.CrossRefPubMed Heitz-Mayfield LJ. Peri-implant diseases: diagnosis and risk indicators. J Clin Periodontol. 2008;35:292–304.CrossRefPubMed
4.
go back to reference Persson GR, Renvert S. Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res. 2014;16:783–93.CrossRefPubMed Persson GR, Renvert S. Cluster of bacteria associated with peri-implantitis. Clin Implant Dent Relat Res. 2014;16:783–93.CrossRefPubMed
5.
go back to reference Heuer W, Kettenring A, Stumpp SN, Eberhard J, Gellermann E, Winkel A, et al. Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig. 2012;16:843–50.CrossRefPubMed Heuer W, Kettenring A, Stumpp SN, Eberhard J, Gellermann E, Winkel A, et al. Metagenomic analysis of the peri-implant and periodontal microflora in patients with clinical signs of gingivitis or mucositis. Clin Oral Investig. 2012;16:843–50.CrossRefPubMed
6.
go back to reference Casado PL, Otazu IB, Balduino A, de Mello W, Barboza EP, Duarte ME. Identification of periodontal pathogens in healthy periimplant sites. Implant Dent. 2011;20:226–35.CrossRefPubMed Casado PL, Otazu IB, Balduino A, de Mello W, Barboza EP, Duarte ME. Identification of periodontal pathogens in healthy periimplant sites. Implant Dent. 2011;20:226–35.CrossRefPubMed
7.
go back to reference Renvert S, Roos-Jansaker AM, Lindahl C, Renvert H, Rutger PG. Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin Oral Implants Res. 2007;18:509–16.CrossRefPubMed Renvert S, Roos-Jansaker AM, Lindahl C, Renvert H, Rutger PG. Infection at titanium implants with or without a clinical diagnosis of inflammation. Clin Oral Implants Res. 2007;18:509–16.CrossRefPubMed
8.
go back to reference Oliveira MA, Carvalho LP, Gomes Mde S, Bacellar O, Barros TF, Carvalho EM. Microbiological and immunological features of oral candidiasis. Microbiol Immunol. 2007;51:713–9.CrossRefPubMed Oliveira MA, Carvalho LP, Gomes Mde S, Bacellar O, Barros TF, Carvalho EM. Microbiological and immunological features of oral candidiasis. Microbiol Immunol. 2007;51:713–9.CrossRefPubMed
9.
go back to reference Leonhardt A, Renvert S, Dahlen G. Microbial findings at failing implants. Clin Oral Implants Res. 1999;10:339–45.CrossRefPubMed Leonhardt A, Renvert S, Dahlen G. Microbial findings at failing implants. Clin Oral Implants Res. 1999;10:339–45.CrossRefPubMed
10.
go back to reference Albertini M, Lopez-Cerero L, O’Sullivan MG, Chereguini CF, Ballesta S, Rios V, et al. Assessment of periodontal and opportunistic flora in patients with peri-implantitis. Clin Oral Implants Res. 2014; Apr 10. doi: 10.1111/clr.12387. [Epub ahead of print] Albertini M, Lopez-Cerero L, O’Sullivan MG, Chereguini CF, Ballesta S, Rios V, et al. Assessment of periodontal and opportunistic flora in patients with peri-implantitis. Clin Oral Implants Res. 2014; Apr 10. doi: 10.1111/clr.12387. [Epub ahead of print]
11.
go back to reference Lang NP, Berglundh T, Working Group 4 of Seventh European Workshop on P. Periimplant diseases: where are we now?--Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38 Suppl 11:178–81.CrossRefPubMed Lang NP, Berglundh T, Working Group 4 of Seventh European Workshop on P. Periimplant diseases: where are we now?--Consensus of the Seventh European Workshop on Periodontology. J Clin Periodontol. 2011;38 Suppl 11:178–81.CrossRefPubMed
12.
go back to reference Henrich B, Schmitt M, Bergmann N, Zanger K, Kubitz R, Haussinger D, et al. Mycoplasma salivarium detected in a microbial community with Candida glabrata in the biofilm of an occluded biliary stent. J Med Microbiol. 2010;59:239–41.CrossRefPubMed Henrich B, Schmitt M, Bergmann N, Zanger K, Kubitz R, Haussinger D, et al. Mycoplasma salivarium detected in a microbial community with Candida glabrata in the biofilm of an occluded biliary stent. J Med Microbiol. 2010;59:239–41.CrossRefPubMed
13.
go back to reference Bizhang M, Ellerbrock B, Preza D, Raab W, Singh P, Beikler T, et al. Detection of nine microorganisms from the initial carious root lesions using a TaqMan-based real-time PCR. Oral Dis. 2011;17:642–52.CrossRefPubMed Bizhang M, Ellerbrock B, Preza D, Raab W, Singh P, Beikler T, et al. Detection of nine microorganisms from the initial carious root lesions using a TaqMan-based real-time PCR. Oral Dis. 2011;17:642–52.CrossRefPubMed
14.
go back to reference McDonald RR, Antonishyn NA, Hansen T, Snook LA, Nagle E, Mulvey MR, et al. Development of a triplex real-time PCR assay for detection of Panton-Valentine leukocidin toxin genes in clinical isolates of methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:6147–9.CrossRefPubMedCentralPubMed McDonald RR, Antonishyn NA, Hansen T, Snook LA, Nagle E, Mulvey MR, et al. Development of a triplex real-time PCR assay for detection of Panton-Valentine leukocidin toxin genes in clinical isolates of methicillin-resistant Staphylococcus aureus. J Clin Microbiol. 2005;43:6147–9.CrossRefPubMedCentralPubMed
15.
go back to reference Morillo JM, Lau L, Sanz M, Herrera D, Martin C, Silva A. Quantitative real-time polymerase chain reaction based on single copy gene sequence for detection of periodontal pathogens. J Clin Periodontol. 2004;31:1054–60.CrossRefPubMed Morillo JM, Lau L, Sanz M, Herrera D, Martin C, Silva A. Quantitative real-time polymerase chain reaction based on single copy gene sequence for detection of periodontal pathogens. J Clin Periodontol. 2004;31:1054–60.CrossRefPubMed
16.
go back to reference Price RR, Viscount HB, Stanley MC, Leung KP. Targeted profiling of oral bacteria in human saliva and in vitro biofilms with quantitative real-time PCR. Biofouling. 2007;23:203–13.CrossRefPubMed Price RR, Viscount HB, Stanley MC, Leung KP. Targeted profiling of oral bacteria in human saliva and in vitro biofilms with quantitative real-time PCR. Biofouling. 2007;23:203–13.CrossRefPubMed
18.
go back to reference Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schaffer AA. Database indexing for production MegaBLAST searches. Bioinformatics. 2008;24:1757–64.CrossRefPubMedCentralPubMed Morgulis A, Coulouris G, Raytselis Y, Madden TL, Agarwala R, Schaffer AA. Database indexing for production MegaBLAST searches. Bioinformatics. 2008;24:1757–64.CrossRefPubMedCentralPubMed
19.
go back to reference Arendorf TM, Walker DM. The prevalence and intra-oral distribution of Candida albicans in man. Arch Oral Biol. 1980;25:1–10.CrossRefPubMed Arendorf TM, Walker DM. The prevalence and intra-oral distribution of Candida albicans in man. Arch Oral Biol. 1980;25:1–10.CrossRefPubMed
20.
go back to reference Helovuo H, Hakkarainen K, Paunio K. Changes in the prevalence of subgingival enteric rods, staphylococci and yeasts after treatment with penicillin and erythromycin. Oral Microbiol Immunol. 1993;8:75–9.CrossRefPubMed Helovuo H, Hakkarainen K, Paunio K. Changes in the prevalence of subgingival enteric rods, staphylococci and yeasts after treatment with penicillin and erythromycin. Oral Microbiol Immunol. 1993;8:75–9.CrossRefPubMed
21.
go back to reference Odden K, Schenck K, Koppang H, Hurlen B. Candidal infection of the gingiva in HIV-infected persons. J Oral Pathol Med. 1994;23:178–83.CrossRefPubMed Odden K, Schenck K, Koppang H, Hurlen B. Candidal infection of the gingiva in HIV-infected persons. J Oral Pathol Med. 1994;23:178–83.CrossRefPubMed
22.
go back to reference Nikawa H, Egusa H, Makihira S, Okamoto T, Kurihara H, Shiba H, et al. An in vitro evaluation of the adhesion of Candida species to oral and lung tissue cells. Mycoses. 2006;49:14–7.CrossRefPubMed Nikawa H, Egusa H, Makihira S, Okamoto T, Kurihara H, Shiba H, et al. An in vitro evaluation of the adhesion of Candida species to oral and lung tissue cells. Mycoses. 2006;49:14–7.CrossRefPubMed
23.
go back to reference Jabra-Rizk MA, Falkler Jr WA, Merz WG, Kelley JI, Baqui AA, Meiller TF. Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J Clin Microbiol. 1999;37:1464–8.PubMedCentralPubMed Jabra-Rizk MA, Falkler Jr WA, Merz WG, Kelley JI, Baqui AA, Meiller TF. Coaggregation of Candida dubliniensis with Fusobacterium nucleatum. J Clin Microbiol. 1999;37:1464–8.PubMedCentralPubMed
24.
go back to reference Thein ZM, Samaranayake YH, Samaranayake LP. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch Oral Biol. 2006;51:672–80.CrossRefPubMed Thein ZM, Samaranayake YH, Samaranayake LP. Effect of oral bacteria on growth and survival of Candida albicans biofilms. Arch Oral Biol. 2006;51:672–80.CrossRefPubMed
25.
go back to reference 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. Clin Oral Implants Res. 2008;19:975–82.CrossRefPubMed 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. Clin Oral Implants Res. 2008;19:975–82.CrossRefPubMed
26.
go back to reference Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B. Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res. 2002;13:349–58.CrossRefPubMed Hultin M, Gustafsson A, Hallstrom H, Johansson LA, Ekfeldt A, Klinge B. Microbiological findings and host response in patients with peri-implantitis. Clin Oral Implants Res. 2002;13:349–58.CrossRefPubMed
27.
go back to reference Engel LD, Kenny GE. Mycoplasma salivarium in human gingival sulci. J Periodontal Res. 1970;5:163–71.CrossRefPubMed Engel LD, Kenny GE. Mycoplasma salivarium in human gingival sulci. J Periodontal Res. 1970;5:163–71.CrossRefPubMed
28.
go back to reference Jarvensivu A, Hietanen J, Rautemaa R, Sorsa T, Richardson M. Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo. Oral Dis. 2004;10:106–12.CrossRefPubMed Jarvensivu A, Hietanen J, Rautemaa R, Sorsa T, Richardson M. Candida yeasts in chronic periodontitis tissues and subgingival microbial biofilms in vivo. Oral Dis. 2004;10:106–12.CrossRefPubMed
29.
go back to reference Reynaud AH, Nygaard-Ostby B, Boygard GK, Eribe ER, Olsen I, Gjermo P. Yeasts in periodontal pockets. J Clin Periodontol. 2001;28:860–4.CrossRefPubMed Reynaud AH, Nygaard-Ostby B, Boygard GK, Eribe ER, Olsen I, Gjermo P. Yeasts in periodontal pockets. J Clin Periodontol. 2001;28:860–4.CrossRefPubMed
30.
go back to reference Canabarro A, Valle C, Farias MR, Santos FB, Lazera M, Wanke B. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013;48:428–32.CrossRefPubMed Canabarro A, Valle C, Farias MR, Santos FB, Lazera M, Wanke B. Association of subgingival colonization of Candida albicans and other yeasts with severity of chronic periodontitis. J Periodontal Res. 2013;48:428–32.CrossRefPubMed
Metadata
Title
Real-time PCR analysis of fungal organisms and bacterial species at peri-implantitis sites
Authors
Frank Schwarz
Kathrin Becker
Sebastian Rahn
Andrea Hegewald
Klaus Pfeffer
Birgit Henrich
Publication date
01-12-2015
Publisher
Springer Berlin Heidelberg
Published in
International Journal of Implant Dentistry / Issue 1/2015
Electronic ISSN: 2198-4034
DOI
https://doi.org/10.1186/s40729-015-0010-6

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