Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The ONWARDS insulin icodec trials

A round-up of the ONWARDS phase 3 clinical trials evaluating the novel weekly insulin icodec in people with diabetes.
ADVANCED SEARCH
Log in
Top
Clinical Oral Investigations
Published in: Clinical Oral Investigations 2/2016

Open Access 01-03-2016 | Original Article

Periodontal pathogens and tetracycline resistance genes in subgingival biofilm of periodontally healthy and diseased Dominican adults

Authors: James R. Collins, Alexandre Arredondo, Alma Roa, Yleana Valdez, Rubén León, Vanessa Blanc

Published in: Clinical Oral Investigations | Issue 2/2016

Login to get access

Abstract

Objective

The objective of this study was to compare the periodontopathogen prevalence and tetracycline resistance genes in Dominican patients with different periodontal conditions.

Methods

Seventy-seven samples were collected from healthy, gingivitis, chronic (CP) and aggressive (AgP) periodontitis patients. Porphyromonas gingivalis, Treponema denticola, Tannerella forsythia, Aggregatibacter actinomycetemcomitans, Fusobacterium nucleatum, Prevotella intermedia, Parvimonas micra, Eikenella corrodens and Dialister pneumosintes and 11 resistance genes were studied by PCR. P. gingivalis fimA genotype was determined.

Results

In healthy patients, P. micra and P. intermedia were the most and least frequently detected, respectively. T. forsythia and E. corrodens appeared in 100 % of gingivitis patients. Red complex, D. pneumosintes and E. corrodens were significantly more prevalent in CP compared to healthy patients. F. nucleatum and T. denticola were detected more frequently in AgP. A. actinomycetemcomitans was the most rarely observed in all groups. The fimA II genotype was the most prevalent in periodontitis patients. Seven tetracycline-resistant genes were detected. tet(Q), tet(32) and tet(W) showed the greatest prevalence. tet(32) was significantly more prevalent in CP than in healthy patients.

Conclusions

Red complex bacteria and D. pneumosintes were significantly the most prevalent species among periodontitis patients. T. forsythia was the most frequently detected in this population. To our knowledge, this is the first study describing the tet(32) gene in subgingival biofilm from healthy and periodontally diseased subjects.

Clinical relevance

This study contributes to the knowledge on the subgingival microbiota and its resistance genes of a scarcely studied world region. Knowing the prevalence of resistance genes could impact on their clinical prescription and could raise awareness to the appropriate use of antibiotics.
Appendix
Available only for authorised users
Literature
1.
Socransky SS (2000) Haffajee AD (2005) Periodontal microbial ecology. Periodontol 38:135–187CrossRef
2.
Rylev M, Kilian M (2008) Prevalence and distribution of principal periodontal pathogens worldwide. J Clin Periodontol 35:346–361CrossRefPubMed
3.
Genco RJ (2000) Borgnakke WS (2013) Risk factors for periodontal disease. Periodontol 62:59–94CrossRef
4.
Haffajee AD, Bogren A, Hasturk H, Feres M, López NJ, Socransky SS (2004) Subgingival microbiota of chronic periodontitis subjects from different geographic locations. J Clin Periodontol 31:996–1002CrossRefPubMed
5.
Sanz M, van Winkelhoff AJ, Herrera D, Dellemijn-Kippuw N, Simón R, Winkel E (2000) Differences in the composition of the subgingival microbiota of two periodontitis populations of different geographical origin. A comparison between Spain and The Netherlands. Eur J Oral Sci 108:383–392CrossRefPubMed
6.
Umeda M, Chen C, Bakker I, Contreras A, Morrison JL, Slots J (1998) Risk indicators for harbouring periodontal pathogens. J Periodontol 69:1111–1118CrossRefPubMed
7.
Mombelli A, Gmür R, Frey J, Meyer J, Zee KY, Tam JO, et al (1998) Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in young Chinese adults. Oral Microbiol Immunol 13:231–237CrossRefPubMed
8.
Haubek D, Ennibi OK, Poulsen K, Poulsen S, Benzarti N, Kilian M (2001) Early-onset periodontitis in Morocco is associated with the highly leukotoxic clone of Actinobacillus actinomycetemcomitans. J Dent Res 80:1580–1583CrossRefPubMed
9.
Tomita S, Komiya-Ito A, Imamura K, Kita D, Ota K, Takamayama S, et al (2013) Prevalence of Aggregatibacter actinomycetemcomitans, Porphyromonas gingivalis and Tannerella forsythia in Japanese patients with generalized chronic and aggressive periodontitis. Microb Pathog 61-62:11–15CrossRefPubMed
10.
Ashimoto A, Chen C, Bakker I, Slots J (1996) Polymerase chain reaction detection of 8 putative periodontal pathogens in subgingival plaque of gingivitis and advanced periodontitis lesions. Oral Microbiol Immunol 11:266–273CrossRefPubMed
11.
Gajardo M, Silva N, Gómez L, León R, Parra B, Contreras A, et al (2005) Prevalence of periodontopathic bacteria in aggressive periodontitis patients in a Chilean population. J Periodontol 76:289–294CrossRefPubMed
12.
Yang HW, Asikainen S, Doğan B, Suda R, Lai CH (2004) Relationship of Actinobacillus actinomycetemcomitans serotype b to aggressive periodontitis: frequency in pure cultured isolates. J Periodontol 75:592–599CrossRefPubMed
13.
Haubek D, Poulsen K, Kilian M (2007) Microevolution and patterns of dissemination of the JP2 clone of Aggregatibacter (Actinobacillus) actinomycetemcomitans. Infect Immun 75:3080–3088PubMedCentralCrossRefPubMed
14.
Aduse-Opoku J, Slaney JM, Hashim A, Gallagher A, Gallagher RP, Rangarajan M, Boutaga K, Laine ML, Van Winkelhoff AJ, Curtis MA (2006) Identification and characterization of the capsular polysaccharide (K-antigen) locus of Porphyromonas gingivalis. Infect Immun 74:449–460PubMedCentralCrossRefPubMed
15.
Kuboniwa M, Inaba H (2000) Amano A (2010) Genotyping to distinguish microbial pathogenicity in periodontitis. Periodontol 54:136–159CrossRef
16.
Amano A, Kubinowa M, Nakagawa I, Akiyama S, Morisaki I, Hamada S (2000) Prevalence of specific genotypes of Porphyromonas gingivalis fimA and periodontal health status. J Dent Res 79:1664–1668CrossRefPubMed
17.
Gilbert P, McBain AJ (2003) Potential impact of increased use of biocides in consumer products on prevalence of antibiotic resistance. Clin Microbiol Rev 16:189–208PubMedCentralCrossRefPubMed
18.
19.
Ardila CM, Granada MI, Guzmán IC (2010) Antibiotic resistance of subgingival species in chronic periodontitis patients. J Periodontal Res 45:557–563PubMed
20.
Veloo AC, Seme K, Raangs E, Rureunga P, Singadji W-MG, et al (2012) Antibiotic susceptibility profiles of oral pathogens. Int J Antimicrob Agents 40:450–454CrossRefPubMed
21.
Chopra I, Roberts M (2001) Tetracycline antibiotics: mode of action, applications, molecular biology, and epidemiology of bacterial resistance. Microbiol Mol Biol Rev 65:232–260PubMedCentralCrossRefPubMed
22.
Herrera D, Alonso B, León R, Roldán S, Sanz M (2008) Antimicrobial therapy in periodontitis: the use of systemic antimicrobials against the subgingival biofilm. J Clin Periodontol 35:45–66CrossRefPubMed
23.
Slots J, Rams TE, Feik D, Taveras HD, Gillespie GM (1991) Subgingival microflora of advanced periodontitis in the Dominican Republic. J Periodontol 62:543–547CrossRefPubMed
24.
Armitage GC (1999) Development of a classification system for periodontal diseases and conditions. Ann Periodontol 4:1–6CrossRefPubMed
25.
Mombelli A, McNabb H, Lang NP (1991) Black-pigmenting Gram-negative bacteria in periodontal disease. II. Screening strategies for detection of P. gingivalis. J Periodontal Res 26:308–313CrossRefPubMed
26.
Doan N, Contreras A, Flynn J, Slots J, Chen C (2000) Molecular identification of Dialister pneumosintes in subgingival plaque of humans. J Clin Microbiol 38:3043–3047PubMedCentralPubMed
27.
Nakagawa I, Amano A, Ohara-Nemoto Y, Endoh N, Morisali I, Kimura S, et al (2002) Identification of a new variant of fimA gene of Porphyromonas gingivalis and its distribution in adults and disabled populations with periodontitis. J Periodontal Res 37:425–432CrossRefPubMed
28.
Aminov RI, Garrigues-Jeanjean N, Mackie RI (2001) Molecular ecology of tetracycline resistance: development and validation of primers for detection of tetracycline resistance genes encoding ribosomal protection proteins. Appl Environ Microbiol 67:22–32PubMedCentralCrossRefPubMed
29.
Warburton P, Roberts AP, Allan E, Seville L, Lancaster H, Mullany P (2009) Characterization of tet(32) genes from the oral metagenome. Antimicrob Agents Chemother 53:273–276PubMedCentralCrossRefPubMed
30.
Ng LK, Martin I, Alfa M, Mulvey M (2001) Multiplex PCR for the detection of tetracycline resistant genes. Mol Cell Probes 15:209–215CrossRefPubMed
31.
Manch-Citron JN, López GH, Dey A, Rapley JW, MacNeill SR, Cobb CM (2000) PCR monitoring for tetracycline resistance genes in subgingival plaque following site-specific periodontal therapy. A preliminary report. J Clin Periodontol 27:437–446CrossRefPubMed
32.
Bojesen AM, Bager RJ, Ifrah D, Aarestrup FM (2011) The rarely reported tet(31) tetracycline resistance determinant is common in Gallibacterium anatis. Vet Microbiol 149:497–499CrossRefPubMed
33.
Botero JE, Contreras A, Lafaurie G, Jaramillo A, Betancourt M, Arce RM (2007) Occurrence of periodontopathic and superinfecting bacteria in chronic and aggressive periodontitis subjects in a Colombian population. J Periodontol 78:696–704CrossRefPubMed
34.
Herrera D, Contreras A, Gamonal J, Oteo A, Jaramillo A, Silva N, et al (2008) Subgingival microbial profiles in chronic periodontitis patients from Chile, Colombia and Spain. J Clin Periodontol 35:106–113CrossRefPubMed
35.
Ledder RG, Gilbert P, Huws SA, Aarons L, Ashley MP, Hull PS, McBain AJ (2007) Molecular analysis of the subgingival microbiota in health and disease. Appl Environ Microbiol 73:516–523PubMedCentralCrossRefPubMed
36.
Torrungruang K, Bandhaya P, Likittanasombat K, Grittayaphong C (2009) Relationship between the presence of certain bacterial pathogens and periodontal status of urban Thai adults. J Periodontol 80:122–129CrossRefPubMed
37.
Riggio MP, Macfarlane TW, Mackenzie D, Lennon A, Smith AJ, Kinane D (1996) Comparison of polymerase chain reaction and culture methods for detection of Actinobacillus actinomycetemcomitans and Porphyromonas gingivalis in subgingival plaque samples. J Periodontal Res 31:496–501CrossRefPubMed
38.
Ali RW, Johannessen AC, Dahlén G, Socransky SS, Skaug N (1997) Comparison of the subgingival microbiota of periodontally healthy and diseased adults in northern Cameroon. J Clin Periodontol 24:830–835CrossRefPubMed
39.
Ferraro CT, Gornic C, Barbosa AS, Peixoto RJ, Colombo AP (2007) Detection of Dialister pneumosintes in the subgingival biofilm of subjects with periodontal disease. Anaerobe 13:244–248CrossRefPubMed
40.
Nonnenmacher C, Dalpke A, Rochon J, Flores-de-Jacoby L, Mutters R, Heeg K (2005) Real-time polymerase chain reaction for detection and quantification of bacteria in periodontal patients. J Periodontol 76:1542–1549CrossRefPubMed
41.
Zambon JJ (1985) Actinobacillus actinomycetemcomitans in human periodontal disease. J Clin Periodontol 12:1–20CrossRefPubMed
42.
Fine DH, Kaplan JB, Kachlany SC (2000) Schreiner HC (2006) How we got attached to Actinobacillus actinomycetemcomitans: a model for infectious diseases. Periodontol 42:114–157CrossRef
43.
Lee JW, Choi BK, Yoo YJ, Choi SH, Cho KS, Chai JK, et al (2003) Distribution of periodontal pathogens in Korean aggressive periodontitis. J Periodontol 74:1329–1335CrossRefPubMed
44.
Tinoco EM, Beldi MI, Loureiro CA (1997) Localized juvenile periodontitis and Actinobacillus actinomycetemcomitans in a Brazilian population. Eur J Oral Sci 105:9–14CrossRefPubMed
45.
Yang HW, Huang YF, Chan Y, Chou MY (2005) Relationship of Actinobacillus actinomycetemcomitans serotypes to periodontal condition: prevalence and proportions in subgingival plaque. Eur J Oral Sci 113:28–33CrossRefPubMed
46.
Guazeli-Amin VH, Avila-Campos MJ, Barbosa DS, Gaetti-Jardim Jr E, Trevisan Jr W, Itano EN (2000) Leukotoxic activity of Actinobacillus actinomycetemcomitans isolated from Brazilian periodontal patients. Anaerobe 6:341–346CrossRef
47.
Gaetti-Jardim Jr E, Wahasugui TC, Tomazinho PH, Marques MM, Nakano V, Avila-Campos MJ (2008) Distribution of biotypes and leukotoxic activity of Aggregatibacter actinomycetemcomitans isolated from Brazilian patients with chronic periodontitis. Braz J Microbiol 39:658–663CrossRefPubMed
48.
Haubek D, Johansson A (2014) Pathogenicity of the highly leukotoxic JP2 clone of Aggregatibacter actinomycetemcomitans and its geographic dissemination and role in aggressive periodontitis. J Oral Microbiol 14:6. doi:10.​3402/​jom.​v6.​23980
49.
Missailidis CG, Emeda JE, Ota-Tsuzuki C, Anzai D, Mayer MPA (2004) Distribution of fimA genotypes of Porphyromonas gingivalis in subjects with various periodontal conditions. Oral Microbiol Immunol 19:224–229CrossRefPubMed
50.
Roberts AP, Mullany P (2010) Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev. Anti-Infect Ther 8:1441–1450CrossRefPubMed
51.
Silfrany RO, Caba RE, de Los S, Santos F, Hanning I (2013) Detection of quinolones in poultry meat obtained from retail centers in Santiago Province, the Dominican Republic. J Food Prot 76:352–354CrossRefPubMed
52.
Silbergeld EK, Graham J, Price LB (2008) Industrial food animal production, antimicrobial resistance, and human health. Annu Rev Public Health 29:151–169CrossRefPubMed
53.
Preshaw PM, Hefti AF, Jepsen S, Etienne D, Walker C, Bradshaw MH (2004) Subantimicrobial dose doxycycline as adjunctive treatment for periodontitis. A review. J Clin Periodontol 31:697–707CrossRefPubMed
54.
Thaker M, Spanogiannopoulos P, Wright GD (2010) The tetracycline resistome. Cell Mol Life Sci 67:419–431CrossRefPubMed
55.
Ioannidis I, Sakellari D, Spala A, Arsenakis M, Konstantinidis A (2009) Prevalence of tetM, tetQ, nim and bla(TEM) genes in the oral cavities of Greek subjects: a pilot study. J Clin Periodontol 36:569–574CrossRefPubMed
56.
Kim SM, Kim HC, Lee SW (2011) Characterization of antibiotic resistance determinants in oral biofilms. J Microbiol 49:595–602CrossRefPubMed
Metadata
Title
Periodontal pathogens and tetracycline resistance genes in subgingival biofilm of periodontally healthy and diseased Dominican adults
Authors
James R. Collins
Alexandre Arredondo
Alma Roa
Yleana Valdez
Rubén León
Vanessa Blanc
Publication date
01-03-2016
Publisher
Springer Berlin Heidelberg
Published in
Clinical Oral Investigations / Issue 2/2016
Print ISSN: 1432-6981
Electronic ISSN: 1436-3771
DOI
https://doi.org/10.1007/s00784-015-1516-2

Other articles of this Issue 2/2016

Clinical Oral Investigations 2/2016 Go to the issue

Original Article

The prognostic value of histopathology on lingual nerve neurosensory recovery after micro-neurosurgery

Short Communication

Irrigant flow during photon-induced photoacoustic streaming (PIPS) using Particle Image Velocimetry (PIV)

Original Article

Interaction of enamel matrix proteins with human periodontal ligament cells

Original Article

Why, when, and how general practitioners restore endodontically treated teeth: a representative survey in Germany

Review

Management of the premaxilla in the treatment of bilateral cleft of lip and palate: what can the literature tell us?

Original Article

Evaluation of a biomarker based blood test for monitoring surgical resection of oral squamous cell carcinomas