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Published in: Clinical Oral Investigations 1/2013

01-01-2013 | Original Article

Oral microbiota in Swiss adolescents

Authors: Sigrun Eick, Malgorzata Pietkiewicz, Anton Sculean

Published in: Clinical Oral Investigations | Issue 1/2013

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Abstract

Objectives

The purpose of the study was to determine the prevalence of different oral microbes in gingival plaque samples and in samples from the dorsum of the tongue in a Swiss adolescent population.

Materials and methods

Ninety-nine adolescents between 15 and 18 years were enrolled. Plaque index, bleeding on probing (BOP), the periodontal screening index, and decayed missed filled tooth (DMFT) index were recorded. Samples from subgingival plaque and swabs from the tongue were analyzed by the Checkerboard DNA-DNA hybridization method. Additionally, counts of Streptococus mutans and Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis, Tannerella forsythia, and Treponema denticola were determined by real-time PCR.

Results

Periodontitis was not diagnosed in any of the subjects but all of them presented signs of gingival inflammation displaying a mean BOP of 28%. Ten (10.1%) subjects were tested positive for P. gingivalis, each 22 (22.2%) for A. actinomycetemcomitans and T. forsythia, (47.5%) for T. denticola. T. denticola and S. mutans showed a high affinity to the gingival plaque, whereas T. forsythia was often detected from the dorsum of the tongue. DMFT was associated with S. mutans counts, and BOP correlated with counts of P. gingivalis and T. denticola.

Conclusions

The present data indicate that: (a) gingivitis but not periodontitis is a common finding among Swiss adolescents, and (b) bacteria associated with periodontitis were frequently detected in the subgingival dental plaque and on the dorsum of the tongue in Swiss adolescents with gingivitis.

Clinical relevance

Although gingivitis was a frequent finding in Swiss adolescents, periodontitis was not detected in this population. The dorsum of the tongue appears to represent an important reservoir for periodontopathic bacteria.
Literature
1.
go back to reference Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38:72–122PubMedCrossRef Holt SC, Ebersole JL (2005) Porphyromonas gingivalis, Treponema denticola, and Tannerella forsythia: the “red complex”, a prototype polybacterial pathogenic consortium in periodontitis. Periodontol 2000 38:72–122PubMedCrossRef
2.
go back to reference (1996) Consensus report. Periodontal diseases: pathogenesis and microbial factors. Ann Periodontol 1:926-32 (1996) Consensus report. Periodontal diseases: pathogenesis and microbial factors. Ann Periodontol 1:926-32
3.
go back to reference Meng S, Zhao L, Yang H, Wu Y, Ouyang Y (2009) Prevalence of Actinobacillus actinomycetemcomitans in Chinese chronic periodontitis patients and periodontally healthy adults. Quintessence Int 40:53–60PubMed Meng S, Zhao L, Yang H, Wu Y, Ouyang Y (2009) Prevalence of Actinobacillus actinomycetemcomitans in Chinese chronic periodontitis patients and periodontally healthy adults. Quintessence Int 40:53–60PubMed
4.
go back to reference Iwano Y, Sugano N, Matsumoto K, Nishihara R, Iizuka T, Yoshinuma N, Ito K (2010) Salivary microbial levels in relation to periodontal status and caries development. J Periodontal Res 45:165–169PubMedCrossRef Iwano Y, Sugano N, Matsumoto K, Nishihara R, Iizuka T, Yoshinuma N, Ito K (2010) Salivary microbial levels in relation to periodontal status and caries development. J Periodontal Res 45:165–169PubMedCrossRef
5.
go back to reference Cortelli JR, Aquino DR, Cortelli SC, Fernandes CB, de Carvalho-Filho J, Franco GC, Costa FO, Kawai T (2008) Etiological analysis of initial colonization of periodontal pathogens in oral cavity. J Clin Microbiol 46:1322–1329PubMedCrossRef Cortelli JR, Aquino DR, Cortelli SC, Fernandes CB, de Carvalho-Filho J, Franco GC, Costa FO, Kawai T (2008) Etiological analysis of initial colonization of periodontal pathogens in oral cavity. J Clin Microbiol 46:1322–1329PubMedCrossRef
6.
go back to reference Kulekci G, Leblebicioglu B, Keskin F, Ciftci S, Badur S (2008) Salivary detection of periodontopathic bacteria in periodontally healthy children. Anaerobe 14:49–54PubMedCrossRef Kulekci G, Leblebicioglu B, Keskin F, Ciftci S, Badur S (2008) Salivary detection of periodontopathic bacteria in periodontally healthy children. Anaerobe 14:49–54PubMedCrossRef
7.
go back to reference Tanner AC, Milgrom PM, Kent R Jr, Mokeem SA, Page RC, Riedy CA, Weinstein P, Bruss J (2002) The microbiota of young children from tooth and tongue samples. J Dent Res 81:53–57PubMedCrossRef Tanner AC, Milgrom PM, Kent R Jr, Mokeem SA, Page RC, Riedy CA, Weinstein P, Bruss J (2002) The microbiota of young children from tooth and tongue samples. J Dent Res 81:53–57PubMedCrossRef
8.
go back to reference Papaioannou W, Gizani S, Haffajee AD, Quirynen M, Mamai-Homata E, Papagiannoulis L (2009) The microbiota on different oral surfaces in healthy children. Oral Microbiol Immunol 24:183–189PubMedCrossRef Papaioannou W, Gizani S, Haffajee AD, Quirynen M, Mamai-Homata E, Papagiannoulis L (2009) The microbiota on different oral surfaces in healthy children. Oral Microbiol Immunol 24:183–189PubMedCrossRef
9.
go back to reference Ashley FP, Gallagher J, Wilson RF (1988) The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, Bacteroides intermedius and spirochaetes in the subgingival microflora of adolescents and their relationship with the amount of supragingival plaque and gingivitis. Oral Microbiol Immunol 3:77–82PubMedCrossRef Ashley FP, Gallagher J, Wilson RF (1988) The occurrence of Actinobacillus actinomycetemcomitans, Bacteroides gingivalis, Bacteroides intermedius and spirochaetes in the subgingival microflora of adolescents and their relationship with the amount of supragingival plaque and gingivitis. Oral Microbiol Immunol 3:77–82PubMedCrossRef
10.
go back to reference Asikainen S, Alaluusua S, Kari K, Kleemola-Kujala E (1986) Subgingival microflora and periodontal conditions in healthy teenagers. J Periodontol 57:505–509PubMedCrossRef Asikainen S, Alaluusua S, Kari K, Kleemola-Kujala E (1986) Subgingival microflora and periodontal conditions in healthy teenagers. J Periodontol 57:505–509PubMedCrossRef
11.
go back to reference Mombelli A, Rutar A, Lang NP (1995) Correlation of the periodontal status 6 years after puberty with clinical and microbiological conditions during puberty. J Clin Periodontol 22:300–305PubMedCrossRef Mombelli A, Rutar A, Lang NP (1995) Correlation of the periodontal status 6 years after puberty with clinical and microbiological conditions during puberty. J Clin Periodontol 22:300–305PubMedCrossRef
12.
go back to reference Cutress TW, Hunter PB, Beck DJ, de Souza P (1978) A comparison of WHO periodontal status index with the periodontal and oral hygiene indices. Community Dent Oral Epidemiol 6:245–252PubMedCrossRef Cutress TW, Hunter PB, Beck DJ, de Souza P (1978) A comparison of WHO periodontal status index with the periodontal and oral hygiene indices. Community Dent Oral Epidemiol 6:245–252PubMedCrossRef
13.
14.
go back to reference Beikler T, Schnitzer S, Abdeen G, Ehmke B, Eisenacher M, Flemmig TF (2006) Sampling strategy for intraoral detection of periodontal pathogens before and following periodontal therapy. J Periodontol 77:1323–1332PubMedCrossRef Beikler T, Schnitzer S, Abdeen G, Ehmke B, Eisenacher M, Flemmig TF (2006) Sampling strategy for intraoral detection of periodontal pathogens before and following periodontal therapy. J Periodontol 77:1323–1332PubMedCrossRef
15.
go back to reference Socransky SS, Smith C, Martin L, Paster BJ, Dewhirst FE, Levin AE (1994) “Checkerboard” DNA-DNA hybridization. Biotechniques 17:788–792PubMed Socransky SS, Smith C, Martin L, Paster BJ, Dewhirst FE, Levin AE (1994) “Checkerboard” DNA-DNA hybridization. Biotechniques 17:788–792PubMed
16.
go back to reference Haffajee AD, Cugini MA, Dibart S, Smith C, Kent RL Jr, Socransky SS (1997) The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol 24:324–334PubMedCrossRef Haffajee AD, Cugini MA, Dibart S, Smith C, Kent RL Jr, Socransky SS (1997) The effect of SRP on the clinical and microbiological parameters of periodontal diseases. J Clin Periodontol 24:324–334PubMedCrossRef
17.
go back to reference Yang JL, Wang MS, Cheng AC, Pan KC, Li CF, Deng SX (2008) A simple and rapid method for extracting bacterial DNA from intestinal microflora for ERIC-PCR detection. World J Gastroenterol 14:2872–2876PubMedCrossRef Yang JL, Wang MS, Cheng AC, Pan KC, Li CF, Deng SX (2008) A simple and rapid method for extracting bacterial DNA from intestinal microflora for ERIC-PCR detection. World J Gastroenterol 14:2872–2876PubMedCrossRef
18.
go back to reference Ximenez-Fyvie LA, Haffajee AD, Socransky SS (2000) Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol 27:722–732PubMedCrossRef Ximenez-Fyvie LA, Haffajee AD, Socransky SS (2000) Microbial composition of supra- and subgingival plaque in subjects with adult periodontitis. J Clin Periodontol 27:722–732PubMedCrossRef
19.
go back to reference Socransky SS, Haffajee AD, Smith C, Martin L, Haffajee JA, Uzel NG, Goodson JM (2004) Use of checkerboard DNA-DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 19:352–362PubMedCrossRef Socransky SS, Haffajee AD, Smith C, Martin L, Haffajee JA, Uzel NG, Goodson JM (2004) Use of checkerboard DNA-DNA hybridization to study complex microbial ecosystems. Oral Microbiol Immunol 19:352–362PubMedCrossRef
20.
go back to reference Eick S, Straube A, Guentsch A, Pfister W, Jentsch H (2011) Comparison of real-time polymerase chain reaction and DNA-strip technology in microbiological evaluation of periodontitis treatment. Diagn Microbiol Infect Dis 69:12–20PubMedCrossRef Eick S, Straube A, Guentsch A, Pfister W, Jentsch H (2011) Comparison of real-time polymerase chain reaction and DNA-strip technology in microbiological evaluation of periodontitis treatment. Diagn Microbiol Infect Dis 69:12–20PubMedCrossRef
21.
go back to reference Yoshida A, Suzuki N, Nakano Y, Kawada M, Oho T, Koga T (2003) Development of a 5′ nuclease-based real-time PCR assay for quantitative detection of cariogenic dental pathogens Streptococcus mutans and Streptococcus sobrinus. J Clin Microbiol 41:4438–4441PubMedCrossRef Yoshida A, Suzuki N, Nakano Y, Kawada M, Oho T, Koga T (2003) Development of a 5′ nuclease-based real-time PCR assay for quantitative detection of cariogenic dental pathogens Streptococcus mutans and Streptococcus sobrinus. J Clin Microbiol 41:4438–4441PubMedCrossRef
22.
go back to reference Slots J, Reynolds HS, Genco RJ (1980) Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun 29:1013–1020PubMed Slots J, Reynolds HS, Genco RJ (1980) Actinobacillus actinomycetemcomitans in human periodontal disease: a cross-sectional microbiological investigation. Infect Immun 29:1013–1020PubMed
23.
go back to reference Umeda M, Miwa Z, Takeuchi Y, Ishizuka M, Huang Y, Noguchi K, Tanaka M, Takagi Y, Ishikawa I (2004) The distribution of periodontopathic bacteria among Japanese children and their parents. J Periodontal Res 39:398–404PubMedCrossRef Umeda M, Miwa Z, Takeuchi Y, Ishizuka M, Huang Y, Noguchi K, Tanaka M, Takagi Y, Ishikawa I (2004) The distribution of periodontopathic bacteria among Japanese children and their parents. J Periodontal Res 39:398–404PubMedCrossRef
24.
go back to reference Dahlen G, Konradsson K, Eriksson S, Teanpaisan R, Piwat S, Carlen A (2010) A microbiological study in relation to the presence of caries and calculus. Acta Odontol Scand 68:199–206PubMedCrossRef Dahlen G, Konradsson K, Eriksson S, Teanpaisan R, Piwat S, Carlen A (2010) A microbiological study in relation to the presence of caries and calculus. Acta Odontol Scand 68:199–206PubMedCrossRef
25.
go back to reference Lamell CW, Griffen AL, McClellan DL, Leys EJ (2000) Acquisition and colonization stability of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in children. J Clin Microbiol 38:1196–1199PubMed Lamell CW, Griffen AL, McClellan DL, Leys EJ (2000) Acquisition and colonization stability of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in children. J Clin Microbiol 38:1196–1199PubMed
26.
go back to reference Socransky SS, Haffajee AD, Smith C, Dibart S (1991) Relation of counts of microbial species to clinical status at the sampled site. J Clin Periodontol 18:766–775PubMedCrossRef Socransky SS, Haffajee AD, Smith C, Dibart S (1991) Relation of counts of microbial species to clinical status at the sampled site. J Clin Periodontol 18:766–775PubMedCrossRef
27.
go back to reference Jentsch H, Cachovan G, Guentsch A, Eickholz P, Pfister W, Eick S (2012) Characterization of Aggregatibacter actinomycetemcomitans strains in periodontitis patients in Germany. Clin Oral Investig. 2012 Jan 14. [Epub ahead of print] Jentsch H, Cachovan G, Guentsch A, Eickholz P, Pfister W, Eick S (2012) Characterization of Aggregatibacter actinomycetemcomitans strains in periodontitis patients in Germany. Clin Oral Investig. 2012 Jan 14. [Epub ahead of print]
28.
go back to reference Kim TS, Frank P, Eickholz P, Eick S, Kim CK (2009) Serotypes of Aggregatibacter actinomycetemcomitans in patients with different ethnic backgrounds. J Periodontol 80:2020–2027PubMedCrossRef Kim TS, Frank P, Eickholz P, Eick S, Kim CK (2009) Serotypes of Aggregatibacter actinomycetemcomitans in patients with different ethnic backgrounds. J Periodontol 80:2020–2027PubMedCrossRef
29.
go back to reference Sirinian G, Shimizu T, Sugar C, Slots J, Chen C (2002) Periodontopathic bacteria in young healthy subjects of different ethnic backgrounds in Los Angeles. J Periodontol 73:283–288PubMedCrossRef Sirinian G, Shimizu T, Sugar C, Slots J, Chen C (2002) Periodontopathic bacteria in young healthy subjects of different ethnic backgrounds in Los Angeles. J Periodontol 73:283–288PubMedCrossRef
30.
go back to reference Bimstein E, Sapir S, Houri-Haddad Y, Dibart S, Van Dyke TE, Shapira L (2004) The relationship between Porphyromonas gingivalis infection and local and systemic factors in children. J Periodontol 75:1371–1376PubMedCrossRef Bimstein E, Sapir S, Houri-Haddad Y, Dibart S, Van Dyke TE, Shapira L (2004) The relationship between Porphyromonas gingivalis infection and local and systemic factors in children. J Periodontol 75:1371–1376PubMedCrossRef
31.
go back to reference Van Assche N, Van Essche M, Pauwels M, Teughels W, Quirynen M (2009) Do periodontopathogens disappear after full-mouth tooth extraction? J Clin Periodontol 36:1043–1047PubMedCrossRef Van Assche N, Van Essche M, Pauwels M, Teughels W, Quirynen M (2009) Do periodontopathogens disappear after full-mouth tooth extraction? J Clin Periodontol 36:1043–1047PubMedCrossRef
32.
go back to reference Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, van Steenberghe D (2004) Impact of tongue cleansers on microbial load and taste. J Clin Periodontol 31:506–510PubMedCrossRef Quirynen M, Avontroodt P, Soers C, Zhao H, Pauwels M, van Steenberghe D (2004) Impact of tongue cleansers on microbial load and taste. J Clin Periodontol 31:506–510PubMedCrossRef
33.
go back to reference Tanaka M, Yamamoto Y, Kuboniwa M, Nonaka A, Nishida N, Maeda K, Kataoka K, Nagata H, Shizukuishi S (2004) Contribution of periodontal pathogens on tongue dorsa analyzed with real-time PCR to oral malodor. Microbes Infect 6:1078–1083PubMedCrossRef Tanaka M, Yamamoto Y, Kuboniwa M, Nonaka A, Nishida N, Maeda K, Kataoka K, Nagata H, Shizukuishi S (2004) Contribution of periodontal pathogens on tongue dorsa analyzed with real-time PCR to oral malodor. Microbes Infect 6:1078–1083PubMedCrossRef
34.
go back to reference Yasukawa T, Ohmori M, Sato S (2010) The relationship between physiologic halitosis and periodontopathic bacteria of the tongue and gingival sulcus. Odontology 98:44–51PubMedCrossRef Yasukawa T, Ohmori M, Sato S (2010) The relationship between physiologic halitosis and periodontopathic bacteria of the tongue and gingival sulcus. Odontology 98:44–51PubMedCrossRef
35.
go back to reference Kanli A, Kanbur NO, Dural S, Derman O (2008) Effects of oral health behaviors and socioeconomic factors on a group of Turkish adolescents. Quintessence Int 39:e26–e32PubMed Kanli A, Kanbur NO, Dural S, Derman O (2008) Effects of oral health behaviors and socioeconomic factors on a group of Turkish adolescents. Quintessence Int 39:e26–e32PubMed
36.
go back to reference Hermann P, Gera I, Borbely J, Fejerdy P, Madlena M (2009) Periodontal health of an adult population in Hungary: findings of a national survey. J Clin Periodontol 36:449–457PubMedCrossRef Hermann P, Gera I, Borbely J, Fejerdy P, Madlena M (2009) Periodontal health of an adult population in Hungary: findings of a national survey. J Clin Periodontol 36:449–457PubMedCrossRef
37.
go back to reference Apatzidou DA, Riggio MP, Kinane DF (2005) Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol 32:973–983PubMedCrossRef Apatzidou DA, Riggio MP, Kinane DF (2005) Impact of smoking on the clinical, microbiological and immunological parameters of adult patients with periodontitis. J Clin Periodontol 32:973–983PubMedCrossRef
38.
go back to reference Van der Velden U, Varoufaki A, Hutter JW, Xu L, Timmerman MF, Van Winkelhoff AJ, Loos BG (2003) Effect of smoking and periodontal treatment on the subgingival microflora. J Clin Periodontol 30:603–610PubMedCrossRef Van der Velden U, Varoufaki A, Hutter JW, Xu L, Timmerman MF, Van Winkelhoff AJ, Loos BG (2003) Effect of smoking and periodontal treatment on the subgingival microflora. J Clin Periodontol 30:603–610PubMedCrossRef
41.
go back to reference Schiffner U, Hoffmann T, Kerschbaum T, Micheelis W (2009) Oral health in German children, adolescents, adults and senior citizens in 2005. Community Dent Health 26:18–22PubMed Schiffner U, Hoffmann T, Kerschbaum T, Micheelis W (2009) Oral health in German children, adolescents, adults and senior citizens in 2005. Community Dent Health 26:18–22PubMed
42.
go back to reference Campus G, Cagetti MG, Senna A, Spano G, Benedicenti S, Sacco G (2009) Differences in oral health among Italian adolescents related to the type of secondary school attended. Oral Health Prev Dent 7:323–330PubMed Campus G, Cagetti MG, Senna A, Spano G, Benedicenti S, Sacco G (2009) Differences in oral health among Italian adolescents related to the type of secondary school attended. Oral Health Prev Dent 7:323–330PubMed
43.
go back to reference Ericsson JS, Abrahamsson KH, Ostberg AL, Hellstrom MK, Jonsson K, Wennstrom JL (2009) Periodontal health status in Swedish adolescents: an epidemiological, cross-sectional study. Swed Dent J 33:131–139PubMed Ericsson JS, Abrahamsson KH, Ostberg AL, Hellstrom MK, Jonsson K, Wennstrom JL (2009) Periodontal health status in Swedish adolescents: an epidemiological, cross-sectional study. Swed Dent J 33:131–139PubMed
44.
go back to reference Rothlisberger B, Kuonen P, Salvi GE, Gerber J, Pjetursson BE, Attstrom R, Joss A, Lang NP (2007) Periodontal conditions in Swiss army recruits: a comparative study between the years 1985, 1996 and 2006. J Clin Periodontol 34:860–866PubMedCrossRef Rothlisberger B, Kuonen P, Salvi GE, Gerber J, Pjetursson BE, Attstrom R, Joss A, Lang NP (2007) Periodontal conditions in Swiss army recruits: a comparative study between the years 1985, 1996 and 2006. J Clin Periodontol 34:860–866PubMedCrossRef
45.
go back to reference Morinushi T, Lopatin DE, Van Poperin N, Ueda Y (2000) The relationship between gingivitis and colonization by Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in children. J Periodontol 71:403–409PubMedCrossRef Morinushi T, Lopatin DE, Van Poperin N, Ueda Y (2000) The relationship between gingivitis and colonization by Porphyromonas gingivalis and Actinobacillus actinomycetemcomitans in children. J Periodontol 71:403–409PubMedCrossRef
46.
go back to reference Timmerman MF, Van der Weijden GA, Arief EM, Armand S, Abbas F, Winkel EG, Van Winkelhoff AJ, Van der Velden U (2001) Untreated periodontal disease in Indonesian adolescents. Subgingival microbiota in relation to experienced progression of periodontitis. J Clin Periodontol 28:617–627PubMedCrossRef Timmerman MF, Van der Weijden GA, Arief EM, Armand S, Abbas F, Winkel EG, Van Winkelhoff AJ, Van der Velden U (2001) Untreated periodontal disease in Indonesian adolescents. Subgingival microbiota in relation to experienced progression of periodontitis. J Clin Periodontol 28:617–627PubMedCrossRef
47.
go back to reference Timmerman MF, Van der Weijden GA, Abbas F, Arief EM, Armand S, Winkel EG, Van Winkelhoff AJ, Van der Velden U (2000) Untreated periodontal disease in Indonesian adolescents. Longitudinal clinical data and prospective clinical and microbiological risk assessment. J Clin Periodontol 27:932–942PubMedCrossRef Timmerman MF, Van der Weijden GA, Abbas F, Arief EM, Armand S, Winkel EG, Van Winkelhoff AJ, Van der Velden U (2000) Untreated periodontal disease in Indonesian adolescents. Longitudinal clinical data and prospective clinical and microbiological risk assessment. J Clin Periodontol 27:932–942PubMedCrossRef
Metadata
Title
Oral microbiota in Swiss adolescents
Authors
Sigrun Eick
Malgorzata Pietkiewicz
Anton Sculean
Publication date
01-01-2013
Publisher
Springer-Verlag
Published in
Clinical Oral Investigations / Issue 1/2013
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-012-0696-2

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