Prevalence and Antibiotic Susceptibility Trends of Selected Enterobacteriaceae, Enterococci, and Candida albicans in the Subgingival Microbiota of German Periodontitis Patients: A Retrospective Surveillance Study

Abstract

The periodontal microbiota is ecologically diverse and may facilitate colonization by bacteria of enteric origin (Enterobacteriaceae, Enterococci) and co-infections with Candida albicans, possibly producing subgingival biofilms with high antimicrobial tolerance. This retrospective surveillance study followed periodontitis-associated superinfection profiles in a large patient sample. From 2008 to 2015, biofilm samples from deep periodontal pockets were collected from a total of 16,612 German adults diagnosed with periodontitis. The presence of selected Enterobacteriaceae, Enterococci, and Candida albicans was confirmed in overnight cultures. Antimicrobial susceptibility of these clinical isolates was tested by disk diffusion with antibiotics routinely used for treatment of oral infections, e.g., amoxicillin (AML), amoxicillin/clavulanic acid (AMC), doxycycline (DO), and ciprofloxacin (CIP). The mean annual prevalence of patients harboring Enterobacteriaceae in periodontal plaques was 11.5% in total and ranged from 2.5% for Enterobacter cloacae to 3.6% for Klebsiella oxytoca, 1.1% for Klebsiella pneumoniae, 2.8% for Serratia marcescens, and 1.5% for Serratia liquefaciens. In comparison, the mean detection rates for microbiota typically found in the oral cavity were higher, e.g., 5.6% for Enterococcus spp. and 21.8% for Candida albicans. Among the Enterobacteriaceae, species harboring intrinsic resistance to AML (Enterobacter spp., Klebsiella spp., Serratia spp.) were predominant. Non-susceptibility to AMC was observed for Serratia spp. and Enterobacter cloacae. By contrast, Enterococcus spp. only showed non-susceptibility to DO and CIP. Trends for increasing resistance were found to AML in Serratia liquefaciens and to DO in Enterococcus spp. Trend analysis showed decreasing resistance to AMC in Serratia liquefaciens and Klebsiella oxytoca; and to DO in Serratia marcescens, liquefaciens, and Enterobacter cloacae. This study confirms the low but consistent presence of Enterobacteriaceae and Enterococci among the subgingival microbiota recovered from periodontitis specimen. Although their pathogenetic role in periodontal lesions remains unclear, their presence in the oral cavity should be recognized as a potential reservoir for development and spread of antibiotic resistance in light of antibiotic usage in oral infections.

Trends and Correlation Between Antimicrobial Resistance and Antibiotics Consumption in a Specialist Children’s Hospital from 2016 to 2021

“…Additionally, biofilm production that could be induced by low-dose, sub-inhibitory, and nonlethal concentrations of antibiotics in various pathogens, including the A. baumannii and E. cloacae , 32–35 which could contribute to increase the tolerance to antibiotics, should be one of multidrug-resistant factors. 36–38 The increasing usage of C/BLI combinations related to the rising carbapenems-resistance rates of A. baumannii corroborates to the previous study; 8 however, the association of consumption of C/BLI combinations with the carbapenems-resistance rates of E. cloacae in our study was inconsistent to that result in the study described previously. 8 As the similar reason analyzed above, the different trends of resistance rates of E.cloacae to carbapenems in the two studies should be the reason of the contradictory result.…”

Ecological Effects of Daily Antiseptic Treatment on Microbial Composition of Saliva-Grown Microcosm Biofilms and Selection of Resistant Phenotypes

“…Apart from these typical oral taxa, Enterobacteriaceae could be isolated from the biofilms from donors 2 and 4. Although members of Enterobacteriaceae are usually considered as transient components of the oral microbiota, they have consistently been detected at low numbers in subgingival biofilm samples ( Espíndola et al, 2022 ; Jepsen et al, 2022 ) and also on toothbrushes ( Zinn et al, 2020 ). For instance, Jepsen et al (2022) recently analyzed biofilm samples collected between 2008 and 2015 from deep periodontal pockets in 16,612 German adults diagnosed with periodontitis and found mean annual prevalence rates of 3.6% for K. oxytoca and 2.5% for E. cloacae .…”

“…Likewise, the resistance of all Enterobacteriaceae isolated in the present study to aminopenicillins such as ampicillin, amoxicillin, and piperacillin and, in part, to second-generation cephalosporins like cefuroxime or cefoxitin may be mainly attributed to their production of AmpC-type beta-lactamases ( Meini et al, 2019 ). Thus, adjunctive prescription of amoxicillin, e.g., in the course of periodontal treatment, may pose the risk of overgrowth of such taxa in oral biofilms ( Jepsen et al, 2022 ). Accordingly, Baker at al.…”

Antibiotika in der parodontalen Therapie

“…Hier spielen insbesondere Infektionen mit Enterobakterien und Enterokokken eine große Rolle, weil diese Erreger hohe Resistenzen gegen Penicillin, Doxycyclin und Chinolone aufweisen. Globale Todesfälle, die auf Antibiotikaresistenzen zurückzuführen sind, liegen besonders hoch bei Klebsiella pneumonia, ein Bakterium, das konsistent auch in der subgingivalen Mikroflora vorkommt, wenn auch in geringer Häufigkeit [30].…”

“…16 000 Parodontitispatienten belegte eine zwar geringe, aber beständige Präsenz von Enterokokken und Enterobacteriaceae im subgingivalen Biofilm. Die Anwesenheit dieser Erreger sollte als potenzielles Reservoir für die Entwicklung und Ausbreitung von antibiotikaresistenten Erregern bedacht werden [30]. Verbessern adjuvante, systemisch verabreichte Antibiotika das klinische Ergebnis der chirurgischen Parodontaltherapie (Stufe 3 der Therapie)?…”