Antibiotic resistance in the microbiota of periodontitis patients: an update of current findings

References

• Aguilar-Luis MA, Casas Apayco L, Tinco Valdez C, De Lama-Odría MDC, Weilg C, Mazulis F, Silva-Caso WG, Del Valle-Mendoza JM. 2021. Screening and assessment of antimicrobial susceptibility of periodontopathic bacteria in peruvian patients with periodontitis: a pilot study. Int J Dent. 2021:2695793.
   PubMed Web of Science ®Google Scholar
• Akrivopoulou C, Green IM, Donos N, Nair SP, Ready D. 2017. Aggregatibacter actinomycetemcomitans serotype prevalence and antibiotic resistance in a UK population with periodontitis. J Glob Antimicrob Resist. 10:54–58.
   PubMed Web of Science ®Google Scholar
• Alauzet C, Lozniewski A, Marchandin H. 2019. Metronidazole resistance and nim genes in anaerobes: a review. Anaerobe. 55:40–53.
   PubMed Web of Science ®Google Scholar
• Almeida VdSM, Azevedo J, Leal HF, Queiroz ATLd, da Silva Filho HP, Reis JN. 2020. Bacterial diversity and prevalence of antibiotic resistance genes in the oral microbiome. PLoS One. 15(9):e0239664.
   PubMed Web of Science ®Google Scholar
• Angarita-Díaz MDP, Bernal-Cepeda L, Bastidas-Legarda L, Forero-Escobar D, Ricaurte-Avendaño A, Mora-Reina J, Vergara-Mercado M, Herrera-Herrera A, Rodriguez-Paz M, Cáceres-Matta S, et al. 2022. Impact of a virtual learning environment on the conscious prescription of antibiotics among Colombian dentists. PLoS One. 17(1):e0262731.
   PubMed Web of Science ®Google Scholar
• Antimicrobial Resistance Collaborators. 2022. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. The Lancet.
   Google Scholar
• Ardila CM, Granada MI, Guzmán IC. 2010. Antibiotic resistance of subgingival species in chronic periodontitis patients. J Periodontal Res. 45(4):557–563.
   PubMed Web of Science ®Google Scholar
• Arredondo A, Blanc V, Mor C, Nart J, León R. 2019. Azithromycin and erythromycin susceptibility and macrolide resistance genes in Prevotella from patients with periodontal disease. Oral Dis. 25(3):860–867.
   PubMed Web of Science ®Google Scholar
• Baquero F, Cantón R, Martinez-Beltrán J, Bolmström A. 1992. The E-test as an epidemiologic tool. Diagn Microbiol Infect Dis. 15(5):483–487.
   PubMed Web of Science ®Google Scholar
• Bartold PM, Van Dyke TE. 2013. Periodontitis: a host-mediated disruption of microbial homeostasis. Unlearning learned concepts. Periodontol 2000. 62(1):203–217.
   PubMed Web of Science ®Google Scholar
• Belibasakis GN, Belstrom D, Eick S, et al. 2023. Periodontal microbiology and microbial etiology of periodontal diseases: historical concepts and contemporary perspectives. Periodontol 2000. doi: 10.1111/prd.12473.
   PubMed Web of Science ®Google Scholar
• Belibasakis GN, Lund BK, Krüger Weiner C, Johannsen B, Baumgartner D, Manoil D, Hultin M, Mitsakakis K. 2020. Healthcare challenges and future solutions in dental practice: assessing oral antibiotic resistances by contemporary point-of-care approaches. Antibiotics. 9(11):810.
   Google Scholar
• Berezow AB, Darveau RP. 2011. Microbial shift and periodontitis. Periodontol 2000. 55(1):36–47.
   PubMed Web of Science ®Google Scholar
• Binta B, Patel M. 2016. Detection of cfxA2, cfxA3, and cfxA6 genes in beta-lactamase producing oral anaerobes. J Appl Oral Sci. 24(2):142–147.
   PubMed Web of Science ®Google Scholar
• Bizzarro S, Laine ML, Buijs MJ, Brandt BW, Crielaard W, Loos BG, Zaura E. 2016. Microbial profiles at baseline and not the use of antibiotics determine the clinical outcome of the treatment of chronic periodontitis. Sci Rep. 6:20205.
   PubMed Web of Science ®Google Scholar
• Buset SL, Zitzmann NU, Weiger R, Walter C. 2015. Non-surgical periodontal therapy supplemented with systemically administered azithromycin: a systematic review of RCTs. Clin Oral Investig. 19(8):1763–1775.
   PubMed Web of Science ®Google Scholar
• Casarin RCV, Peloso Ribeiro ED, Sallum EA, Nociti FH, Gonçalves RB, Casati MZ. 2012. The combination of amoxicillin and metronidazole improves clinical and microbiologic results of one-stage, full-mouth, ultrasonic debridement in aggressive periodontitis treatment. J Periodontol. 83(8):988–998.
   PubMed Web of Science ®Google Scholar
• Citterio F, Gualini G, Chang M, Piccoli GM, Giraudi M, Manavella V, Baima G, Mariani GM, Romano F, Aimetti M, et al. 2022. Pocket closure and residual pockets after non-surgical periodontal therapy: a systematic review and meta-analysis. J Clin Periodontol. 49(1):2–14.
   PubMed Web of Science ®Google Scholar
• Collins JR, Arredondo A, Roa A, Valdez Y, León R, Blanc V. 2016. Periodontal pathogens and tetracycline resistance genes in subgingival biofilm of periodontally healthy and diseased Dominican adults. Clin Oral Investig. 20(2):349–356.
   PubMed Web of Science ®Google Scholar
• Cooper L, Sneddon J, Thompson W, et al. 2022. Tackling antimicrobial resistance in practice: dental students’ evaluation of university teaching supplemented by an online course. JAC Antimicrob Resist. 4(2):dlac039.
   PubMedGoogle Scholar
• Cosgarea R, Jepsen S, Heumann C, et al. 2022. Clinical, microbiological, and immunological effects of 3- or 7-day systemic antibiotics adjunctive to subgingival instrumentation in patients with aggressive (Stage III/IV Grade C) periodontitis: a randomized placebo-controlled clinical trial. J Clin Periodontol. 49(11):1106-1120.
   PubMed Web of Science ®Google Scholar
• Cosgarea R, Juncar R, Heumann C, Tristiu R, Lascu L, Arweiler N, Stavropoulos A, Sculean A. 2016. Non-surgical periodontal treatment in conjunction with 3 or 7 days systemic administration of amoxicillin and metronidazole in severe chronic periodontitis patients. A placebo-controlled randomized clinical study. J Clin Periodontol. 43(9):767–777.
   PubMed Web of Science ®Google Scholar
• Dahlen G, Preus HR. 2017. Low antibiotic resistance among anaerobic Gram-negative bacteria in periodontitis 5 years following metronidazole therapy. Anaerobe. 43:94–98.
   PubMed Web of Science ®Google Scholar
• Dashti AA, Jadaon MM, Habeeb FM. 2009. Can we rely on one laboratory test in detection of extended-spectrum beta-lactamases among Enterobacteriaceae? An evaluation of the Vitek 2 system and comparison with four other detection methods in Kuwait. J Clin Pathol. 62(8):739–742.
   PubMed Web of Science ®Google Scholar
• Dawson-Hahn EE, Mickan S, Onakpoya I, Roberts N, Kronman M, Butler CC, Thompson MJ. 2017. Short-course versus long-course oral antibiotic treatment for infections treated in outpatient settings: a review of systematic reviews. Fam Pract. 34(5):511–519.
   PubMed Web of Science ®Google Scholar
• Emmott R, Barber SK, Thompson W. 2021. Antibiotics and toothache: a social media review. Int J Pharm Pract. 29(3):210–217.
   PubMed Web of Science ®Google Scholar
• Guerrero A, Nibali L, Lambertenghi R, Ready D, Suvan J, Griffiths GS, Wilson M, Tonetti MS. 2014. Impact of baseline microbiological status on clinical outcomes in generalized aggressive periodontitis patients treated with or without adjunctive amoxicillin and metronidazole: an exploratory analysis from a randomized controlled clinical trial. J Clin Periodontol. 41(11):1080–1089.
   PubMed Web of Science ®Google Scholar
• Harks I, Koch R, Eickholz P, Hoffmann T, Kim T-S, Kocher T, Meyle J, Kaner D, Schlagenhauf U, Doering S, et al. 2015. Is progression of periodontitis relevantly influenced by systemic antibiotics? A clinical randomized trial. J Clin Periodontol. 42(9):832–842.
   PubMed Web of Science ®Google Scholar
• International Organisation for Standardisation. 2019. Susceptibility testing of infectious agents and evaluation of performance of antimicrobial susceptibility test devices. Part 1: broth micro-dilution reference method for testing the in vitro activity of antimicrobial agents against rapidly growing aerobic bacteria involved in infection diseases.
   Google Scholar
• Japoni A, Vasin A, Noushadi S, Kiany F, Japoni S, Alborzi A. 2011. Antibacterial susceptibility patterns of Porphyromonas gingivalis isolated from chronic periodontitis patients. Med Oral Patol Oral Cir Bucal. 16(7):e1031-5–e1035.
   PubMed Web of Science ®Google Scholar
• Jepsen K, Falk W, Brune F, Fimmers R, Jepsen S, Bekeredjian-Ding I. 2021. Prevalence and antibiotic susceptibility trends of periodontal pathogens in the subgingival microbiota of German periodontitis patients: a retrospective surveillance study. J Clin Periodontol. 48(9):1216–1227.
   PubMed Web of Science ®Google Scholar
• Jiao J, Zhang L, Meng H-X, Shi D, Lu R-F, Xu L, Feng X-H, Cao Z-Q. 2018. Clinical performance of non-surgical periodontal therapy in a large Chinese population with generalized aggressive periodontitis. J Clin Periodontol. 45(10):1184–1197.
   PubMed Web of Science ®Google Scholar
• Keestra JAJ, Grosjean I, Coucke W, Quirynen M, Teughels W. 2015. Non-surgical periodontal therapy with systemic antibiotics in patients with untreated chronic periodontitis: a systematic review and meta-analysis. J Periodontal Res. 50(3):294–314.
   PubMed Web of Science ®Google Scholar
• Klein EY, Milkowska-Shibata M, Tseng KK, Sharland M, Gandra S, Pulcini C, Laxminarayan R. 2021. Assessment of WHO antibiotic consumption and access targets in 76 countries, 2000-15: an analysis of pharmaceutical sales data. Lancet Infect Dis. 21(1):107–115.
   PubMed Web of Science ®Google Scholar
• Kopra E, Lahdentausta L, Pietiäinen M, Buhlin K, Mäntylä P, Hörkkö S, Persson R, Paju S, Sinisalo J, Salminen A, et al. 2021. Systemic antibiotics influence periodontal parameters and oral microbiota, but not serological markers. Front Cell Infect Microbiol. 11:774665.
   PubMed Web of Science ®Google Scholar
• Kuboniwa M, Lamont RJ. 2010. Subgingival biofilm formation. Periodontol 2000. 52(1):38–52.
   PubMedGoogle Scholar
• Li YH, Tian X. 2012. Quorum sensing and bacterial social interactions in biofilms. Sensors (Basel). 12(3):2519–2538.
   PubMed Web of Science ®Google Scholar
• Lim JM, Singh SR, Duong MC, Legido-Quigley H, Hsu LY, Tam CC. 2020. Impact of national interventions to promote responsible antibiotic use: a systematic review. J Antimicrob Chemother. 75(1):14–29.
   PubMed Web of Science ®Google Scholar
• Lu H, He L, Jin D, et al. 2021. Effect of adjunctive systemic antibiotics on microbial populations compared with scaling and root planing alone for the treatment of periodontitis: a pilot randomized clinical trial. J Periodontol. 93(4):570-583.
   PubMed Web of Science ®Google Scholar
• Lum EPM, Page K, Nissen L, Doust J, Graves N. 2017. Australian consumer perspectives, attitudes and behaviours on antibiotic use and antibiotic resistance: a qualitative study with implications for public health policy and practice. BMC Public Health. 17(1):799.
   PubMedGoogle Scholar
• Maalej SM, Meziou MR, Rhimi FM, Hammami A. 2011. Comparison of disc diffusion, Etest and agar dilution for susceptibility testing of colistin against Enterobacteriaceae. Lett Appl Microbiol. 53(5):546–551.
   PubMed Web of Science ®Google Scholar
• Matarazzo F, Figueiredo LC, Cruz SEB, Faveri M, Feres M. 2008. Clinical and microbiological benefits of systemic metronidazole and amoxicillin in the treatment of smokers with chronic periodontitis: a randomized placebo-controlled study. J Clin Periodontol. 35(10):885–896.
   PubMed Web of Science ®Google Scholar
• Miller BJ, Carson KA, Keller S. 2020. Educating patients on unnecessary antibiotics: personalizing potential harm aids patient understanding. J Am Board Fam Med. 33(6):969–977.
   PubMed Web of Science ®Google Scholar
• Miranda TS, Feres M, Perez-Chaparro PJ, Faveri M, Figueiredo LC, Tamashiro NS, Bastos MF, Duarte PM. 2014. Metronidazole and amoxicillin as adjuncts to scaling and root planing for the treatment of type 2 diabetic subjects with periodontitis: 1-year outcomes of a randomized placebo-controlled clinical trial. J Clin Periodontol. 41(9):890–899.
   PubMed Web of Science ®Google Scholar
• Mombelli A, Schmid B, Rutar A, Lang NP. 2000. Persistence patterns of Porphyromonas gingivalis, Prevotella intermedia/nigrescens, and Actinobacillus actinomyetemcomitans after mechanical therapy of periodontal disease. J Periodontol. 71(1):14–21.
   PubMed Web of Science ®Google Scholar
• Munck C, Sheth RU, Cuaresma E, Weidler J, Stump SL, Zachariah P, Chong DH, Uhlemann A-C, Abrams JA, Wang HH, et al. 2020. The effect of short-course antibiotics on the resistance profile of colonizing gut bacteria in the ICU: a prospective cohort study. Crit Care. 24(1):404.
   PubMed Web of Science ®Google Scholar
• Ng E, Tay JRH, Balan P, Ong MMA, Bostanci N, Belibasakis GN, Seneviratne CJ. 2021. Metagenomic sequencing provides new insights into the subgingival bacteriome and aetiopathology of periodontitis. J Periodontal Res. 56(2):205–218.
   PubMed Web of Science ®Google Scholar
• Ng E, Tay JRH, Ong MMA. 2021. Minimally invasive periodontology: a treatment philosophy and suggested approach. Int J Dent. 2021:2810264.
   PubMed Web of Science ®Google Scholar
• Nibali L, Koidou VP, Hamborg T, Donos N. 2019. Empirical or microbiologically guided systemic antimicrobials as adjuncts to non-surgical periodontal therapy? A systematic review. J Clin Periodontol. 46(10):999–1012.
   PubMed Web of Science ®Google Scholar
• O’Neill J. 2022. Antimicrobial resistance: tackling a crisis for the health and wealth of nations, 2014. [accessed 2022 Jan 15]. https://amr-review.org/sites/default/files/AMR%20Review%20Paper%20-%20Tackling%20a%20crisis%20for%20the%20health%20and%20wealth%20of%20nations_1.pdf.
   Google Scholar
• O’Rourke VJ. 2017. Azithromycin as an adjunct to non-surgical periodontal therapy: a systematic review. Aust Dent J. 62(1):14–22.
   PubMed Web of Science ®Google Scholar
• Pérez-Amate B, Figueiredo R, Cortés-Peral S, Sánchez-Torres A, Valmaseda-Castellón E. 2021. Patient perception about the need for antibiotics after tooth extractions: a cross-sectional study. J Clin Exp Dent. 13(5):e499–e504.
   PubMedGoogle Scholar
• Rams TE, Degener JE, van Winkelhoff AJ. 2013. Prevalence of β-lactamase-producing bacteria in human periodontitis. J Periodontal Res. 48(4):493–499.
   PubMed Web of Science ®Google Scholar
• Rams TE, Degener JE, van Winkelhoff AJ. 2014. Antibiotic resistance in human chronic periodontitis microbiota. J Periodontol. 85(1):160–169.
   PubMed Web of Science ®Google Scholar
• Rams TE, Dujardin S, Sautter JD, Degener JE, van Winkelhoff AJ. 2011. Spiramycin resistance in human periodontitis microbiota. Anaerobe. 17(4):201–205.
   PubMed Web of Science ®Google Scholar
• Rams TE, Feik D, Mortensen JE, Degener JE, van Winkelhoff AJ. 2014. Antibiotic susceptibility of periodontal Streptococcus constellatus and Streptococcus intermedius clinical isolates. J Periodontol. 85(12):1792–1798.
   PubMed Web of Science ®Google Scholar
• Rams TE, Sautter JD, van Winkelhoff AJ. 2020a. Antibiotic resistance of human periodontal pathogen parvimonas micra over 10 years. Antibiotics (Basel). 9(10):709.
   PubMed Web of Science ®Google Scholar
• Rams TE, Sautter JD, van Winkelhoff AJ. 2020b. Comparative in vitro resistance of human periodontal bacterial pathogens to tinidazole and four other antibiotics. Antibiotics (Basel). 9(2):68.
   PubMed Web of Science ®Google Scholar
• Roberts AP, Mullany P. 2010. Oral biofilms: a reservoir of transferable, bacterial, antimicrobial resistance. Expert Rev anti Infect Ther. 8(12):1441–1450.
   PubMed Web of Science ®Google Scholar
• Sabuncu E, David J, Bernède-Bauduin C, Pépin S, Leroy M, Boëlle P-Y, Watier L, Guillemot D. 2009. Significant reduction of antibiotic use in the community after a nationwide campaign in France, 2002–2007. PLoS Med. 6(6):e1000084.
   PubMed Web of Science ®Google Scholar
• Sgolastra F, Gatto R, Petrucci A, Monaco A. 2012. Effectiveness of systemic amoxicillin/metronidazole as adjunctive therapy to scaling and root planing in the treatment of chronic periodontitis: a systematic review and meta-analysis. J Periodontol. 83(10):1257–1269.
   PubMed Web of Science ®Google Scholar
• Sgolastra F, Petrucci A, Ciarrocchi I, Masci C, Spadaro A. 2021. Adjunctive systemic antimicrobials in the treatment of chronic periodontitis: a systematic review and network meta-analysis. J Periodontal Res. 56(2):236–248.
   PubMed Web of Science ®Google Scholar
• Shlezinger M, Khalifa L, Houri-Haddad Y, Coppenhagen-Glazer S, Resch G, Que Y-A, Beyth S, Dorfman E, Hazan R, Beyth N, et al. 2017. Phage therapy: a new horizon in the antibacterial treatment of oral pathogens. Curr Top Med Chem. 17(10):1199–1211.
   PubMed Web of Science ®Google Scholar
• Silva MP, Feres M, Sirotto TAO, Soares GMS, Mendes JAV, Faveri M, Figueiredo LC. 2011. Clinical and microbiological benefits of metronidazole alone or with amoxicillin as adjuncts in the treatment of chronic periodontitis: a randomized placebo-controlled clinical trial. J Clin Periodontol. 38(9):828–837.
   PubMed Web of Science ®Google Scholar
• Singh N, Rogers P, Atwood CW, Wagener MM, Yu VL. 2000. Short-course empiric antibiotic therapy for patients with pulmonary infiltrates in the intensive care unit. A proposed solution for indiscriminate antibiotic prescription. Am J Respir Crit Care Med. 162(2 Pt 1):505–511.
   PubMed Web of Science ®Google Scholar
• Soares GMS, Figueiredo LC, Faveri M, Cortelli SC, Duarte PM, Feres M. 2012. Mechanisms of action of systemic antibiotics used in periodontal treatment and mechanisms of bacterial resistance to these drugs. J Appl Oral Sci. 20(3):295–309.
   PubMed Web of Science ®Google Scholar
• Soares GMS, Mendes JAV, Silva MP, Faveri M, Teles R, Socransky SS, Wang X, Figueiredo LC, Feres M. 2014. Metronidazole alone or with amoxicillin as adjuncts to non-surgical treatment of chronic periodontitis: a secondary analysis of microbiological results from a randomized clinical trial. J Clin Periodontol. 41(4):366–376.
   PubMed Web of Science ®Google Scholar
• Socransky SS, Haffajee AD. 2002. Dental biofilms: difficult therapeutic targets. Periodontol 2000. 28:12–55.
   PubMed Web of Science ®Google Scholar
• Tamashiro NS, Duarte PM, Miranda TS, Maciel SS, Figueiredo LC, Faveri M, Feres M. 2016. Amoxicillin plus metronidazole therapy for patients with periodontitis and type 2 diabetes: a 2-year randomized controlled trial. J Dent Res. 95(7):829–836.
   PubMed Web of Science ®Google Scholar
• Teughels W, Feres M, Oud V, Martín C, Matesanz P, Herrera D. 2020. Adjunctive effect of systemic antimicrobials in periodontitis therapy: a systematic review and meta-analysis. J Clin Periodontol. 47 Suppl 22(Suppl 22):257–281.
   PubMedGoogle Scholar
• Thompson W, Williams D, Pulcini C, et al. 2020. The essential role of the dental team in reducing antibiotic resistance. Geneva: FDI World Dental Federation.
   Google Scholar
• Thornhill MH, Dayer MJ, Prendergast B, Baddour LM, Jones S, Lockhart PB. 2015. Incidence and nature of adverse reactions to antibiotics used as endocarditis prophylaxis. J Antimicrob Chemother. 70(8):2382–2388.
   PubMed Web of Science ®Google Scholar
• Turnidge J, Paterson DL. 2007. Setting and revising antibacterial susceptibility breakpoints. Clin Microbiol Rev. 20(3):391–408, table of contents.
   PubMed Web of Science ®Google Scholar
• Van der Weijden GAF, Dekkers GJ, Slot DE. 2019. Success of non-surgical periodontal therapy in adult periodontitis patients: a retrospective analysis. Int J Dent Hyg. 17(4):309–317.
   PubMed Web of Science ®Google Scholar
• van Winkelhoff AJ, Herrera D, Oteo A, Sanz M. 2005. Antimicrobial profiles of periodontal pathogens isolated from periodontitis patients in The Netherlands and Spain. J Clin Periodontol. 32(8):893–898.
   PubMed Web of Science ®Google Scholar
• van Winkelhoff AJ, Herrera Gonzales D, Winkel EG, Dellemijn-Kippuw N, Vandenbroucke-Grauls CM, Sanz M. 2000. Antimicrobial resistance in the subgingival microflora in patients with adult periodontitis. A comparison between The Netherlands and Spain. J Clin Periodontol. 27(2):79–86.
   PubMed Web of Science ®Google Scholar
• Veloo ACM, Seme K, Raangs E, Rurenga P, Singadji Z, Wekema-Mulder G, van Winkelhoff AJ. 2012. Antibiotic susceptibility profiles of oral pathogens. Int J Antimicrob Agents. 40(5):450–454.
   PubMed Web of Science ®Google Scholar
• Vrijghem C, Cosyn J, Fransen J, Christiaens V. 2021. A questionnaire-based crossover study on the association of microbiological testing with prescription of systemic antibiotics following initial periodontal therapy. J Clin Periodontol. 48(5):618–626.
   PubMed Web of Science ®Google Scholar
• World Health Organisation. 2022. WHO strategic priorities on antimicrobial resistance 2022. [accessed 2022 Feb 14].
   Google Scholar
• World Health Organisation. Antimicrobial resistance 2021 [accessed 2021 Dec 31]. https://www.who.int/news-room/fact-sheets/detail/antimicrobial-resistance.
   Google Scholar
• Zandbergen D, Slot DE, Cobb CM, Van der Weijden FA. 2013. The clinical effect of scaling and root planing and the concomitant administration of systemic amoxicillin and metronidazole: a systematic review. J Periodontol. 84(3):332–351.
   PubMed Web of Science ®Google Scholar
• Zandbergen D, Slot DE, Niederman R, Van der Weijden FA. 2016. The concomitant administration of systemic amoxicillin and metronidazole compared to scaling and root planing alone in treating periodontitis: =a systematic review=. BMC Oral Health. 16:27.
   PubMed Web of Science ®Google Scholar
• Zhao H, Hu J, Zhao L. 2021. The effect of drug dose and duration of adjuvant Amoxicillin-plus-Metronidazole to full-mouth scaling and root planing in periodontitis: a systematic review and meta-analysis. Clin Oral Investig. 25(10):5671–5685.
   PubMed Web of Science ®Google Scholar