Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis

Detalhes bibliográficos
Autor(a) principal: Costa, Carolina F. F. A.
Data de Publicação: 2021
Outros Autores: Merino-Ribas, Ana, Ferreira, Catarina, Campos, Carla, Silva, Nádia, Pereira, Luciano, Garcia, Andreia, Azevedo, Álvaro, Mesquita, Raquel B. R., Rangel, António O. S. S., Manaia, Célia M., Sampaio-Maia, Benedita
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: http://hdl.handle.net/10400.14/36349
Resumo: Chronic Kidney Disease (CKD) is a growing public-health concern worldwide. Patients exhibit compromised immunity and are more prone to infection than other populations. Therefore, oral colonization by clinically relevant members of the Enterobacteriaceae family, major agents of both nosocomial and dialysis-associated infections with frequent prevalence of antibiotic resistances, may constitute a serious risk. Thus, this study aimed to assess the occurrence of clinically relevant enterobacteria and their antibiotic resistance profiles in the oral cavity of CKD patients undergoing peritoneal dialysis (CKD-PD) and compare it to healthy controls. Saliva samples from all the participants were cultured on MacConkey Agar and evaluated regarding the levels of urea, ammonia, and pH. Bacterial isolates were identified and characterized for antibiotic resistance phenotype and genotype. The results showed that CKD-PD patients exhibited significantly higher salivary pH, urea, and ammonia levels than controls, that was accompanied by higher prevalence and diversity of oral enterobacteria. Out of all the species isolated, only the prevalence of Raoultella ornithinolytica varied significantly between groups, colonizing the oral cavity of approximately 30% of CKD-PD patients while absent from controls. Antibiotic resistance phenotyping revealed mostly putative intrinsic resistance phenotypes (to amoxicillin, ticarcillin, and cephalothin), and resistance to sulfamethoxazole (~43% of isolates) and streptomycin (~17%). However, all isolates were resistant to at least one of the antibiotics tested and multidrug resistance isolates were only found in CKD-PD group (31,6%). Mobile genetic elements and resistance genes were detected in isolates of the species Raoultella ornithinolytica, Klebsiella pneumoniae, Klebsiella oxytoca, Escherichia coli, and Enterobacter asburiae, mostly originated from CKD-PD patients. PD-related infection history revealed that Enterobacteriaceae were responsible for ~8% of peritonitis and ~ 16% of exit-site infections episodes in CKD-PD patients, although no association was found to oral enterobacteria colonization at the time of sampling. The results suggest that the CKD-induced alterations of the oral milieu might promote a dysbiosis of the commensal oral microbiome, namely the proliferation of clinically relevant Enterobacteriaceae potentially harboring acquired antibiotic resistance genes. This study highlights the importance of the oral cavity as a reservoir for pathobionts and antibiotic resistances in CKD patients undergoing peritoneal dialysis.
id RCAP_edaf8f41e18d2343e3cea193a54051c5
oai_identifier_str oai:repositorio.ucp.pt:10400.14/36349
network_acronym_str RCAP
network_name_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository_id_str 7160
spelling Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysisAntibiotic resistanceChronic kidney diseaseEnterobacteriaceaeOral dysbiosisOral microbiomePeritoneal dialysisRaoultella ornithinolyticaChronic Kidney Disease (CKD) is a growing public-health concern worldwide. Patients exhibit compromised immunity and are more prone to infection than other populations. Therefore, oral colonization by clinically relevant members of the Enterobacteriaceae family, major agents of both nosocomial and dialysis-associated infections with frequent prevalence of antibiotic resistances, may constitute a serious risk. Thus, this study aimed to assess the occurrence of clinically relevant enterobacteria and their antibiotic resistance profiles in the oral cavity of CKD patients undergoing peritoneal dialysis (CKD-PD) and compare it to healthy controls. Saliva samples from all the participants were cultured on MacConkey Agar and evaluated regarding the levels of urea, ammonia, and pH. Bacterial isolates were identified and characterized for antibiotic resistance phenotype and genotype. The results showed that CKD-PD patients exhibited significantly higher salivary pH, urea, and ammonia levels than controls, that was accompanied by higher prevalence and diversity of oral enterobacteria. Out of all the species isolated, only the prevalence of Raoultella ornithinolytica varied significantly between groups, colonizing the oral cavity of approximately 30% of CKD-PD patients while absent from controls. Antibiotic resistance phenotyping revealed mostly putative intrinsic resistance phenotypes (to amoxicillin, ticarcillin, and cephalothin), and resistance to sulfamethoxazole (~43% of isolates) and streptomycin (~17%). However, all isolates were resistant to at least one of the antibiotics tested and multidrug resistance isolates were only found in CKD-PD group (31,6%). Mobile genetic elements and resistance genes were detected in isolates of the species Raoultella ornithinolytica, Klebsiella pneumoniae, Klebsiella oxytoca, Escherichia coli, and Enterobacter asburiae, mostly originated from CKD-PD patients. PD-related infection history revealed that Enterobacteriaceae were responsible for ~8% of peritonitis and ~ 16% of exit-site infections episodes in CKD-PD patients, although no association was found to oral enterobacteria colonization at the time of sampling. The results suggest that the CKD-induced alterations of the oral milieu might promote a dysbiosis of the commensal oral microbiome, namely the proliferation of clinically relevant Enterobacteriaceae potentially harboring acquired antibiotic resistance genes. This study highlights the importance of the oral cavity as a reservoir for pathobionts and antibiotic resistances in CKD patients undergoing peritoneal dialysis.Veritati - Repositório Institucional da Universidade Católica PortuguesaCosta, Carolina F. F. A.Merino-Ribas, AnaFerreira, CatarinaCampos, CarlaSilva, NádiaPereira, LucianoGarcia, AndreiaAzevedo, ÁlvaroMesquita, Raquel B. R.Rangel, António O. S. S.Manaia, Célia M.Sampaio-Maia, Benedita2022-01-04T15:45:33Z2021-12-142021-12-14T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttp://hdl.handle.net/10400.14/36349eng1664-302X10.3389/fmicb.2021.73668585121861915PMC871374234970231000737518800001info:eu-repo/semantics/openAccessreponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãoinstacron:RCAAP2023-12-05T01:37:35Zoai:repositorio.ucp.pt:10400.14/36349Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T18:29:32.920966Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informaçãofalse
dc.title.none.fl_str_mv Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
title Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
spellingShingle Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
Costa, Carolina F. F. A.
Antibiotic resistance
Chronic kidney disease
Enterobacteriaceae
Oral dysbiosis
Oral microbiome
Peritoneal dialysis
Raoultella ornithinolytica
title_short Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
title_full Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
title_fullStr Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
title_full_unstemmed Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
title_sort Characterization of oral enterobacteriaceae prevalence and resistance profile in chronic kidney disease patients undergoing peritoneal dialysis
author Costa, Carolina F. F. A.
author_facet Costa, Carolina F. F. A.
Merino-Ribas, Ana
Ferreira, Catarina
Campos, Carla
Silva, Nádia
Pereira, Luciano
Garcia, Andreia
Azevedo, Álvaro
Mesquita, Raquel B. R.
Rangel, António O. S. S.
Manaia, Célia M.
Sampaio-Maia, Benedita
author_role author
author2 Merino-Ribas, Ana
Ferreira, Catarina
Campos, Carla
Silva, Nádia
Pereira, Luciano
Garcia, Andreia
Azevedo, Álvaro
Mesquita, Raquel B. R.
Rangel, António O. S. S.
Manaia, Célia M.
Sampaio-Maia, Benedita
author2_role author
author
author
author
author
author
author
author
author
author
author
dc.contributor.none.fl_str_mv Veritati - Repositório Institucional da Universidade Católica Portuguesa
dc.contributor.author.fl_str_mv Costa, Carolina F. F. A.
Merino-Ribas, Ana
Ferreira, Catarina
Campos, Carla
Silva, Nádia
Pereira, Luciano
Garcia, Andreia
Azevedo, Álvaro
Mesquita, Raquel B. R.
Rangel, António O. S. S.
Manaia, Célia M.
Sampaio-Maia, Benedita
dc.subject.por.fl_str_mv Antibiotic resistance
Chronic kidney disease
Enterobacteriaceae
Oral dysbiosis
Oral microbiome
Peritoneal dialysis
Raoultella ornithinolytica
topic Antibiotic resistance
Chronic kidney disease
Enterobacteriaceae
Oral dysbiosis
Oral microbiome
Peritoneal dialysis
Raoultella ornithinolytica
description Chronic Kidney Disease (CKD) is a growing public-health concern worldwide. Patients exhibit compromised immunity and are more prone to infection than other populations. Therefore, oral colonization by clinically relevant members of the Enterobacteriaceae family, major agents of both nosocomial and dialysis-associated infections with frequent prevalence of antibiotic resistances, may constitute a serious risk. Thus, this study aimed to assess the occurrence of clinically relevant enterobacteria and their antibiotic resistance profiles in the oral cavity of CKD patients undergoing peritoneal dialysis (CKD-PD) and compare it to healthy controls. Saliva samples from all the participants were cultured on MacConkey Agar and evaluated regarding the levels of urea, ammonia, and pH. Bacterial isolates were identified and characterized for antibiotic resistance phenotype and genotype. The results showed that CKD-PD patients exhibited significantly higher salivary pH, urea, and ammonia levels than controls, that was accompanied by higher prevalence and diversity of oral enterobacteria. Out of all the species isolated, only the prevalence of Raoultella ornithinolytica varied significantly between groups, colonizing the oral cavity of approximately 30% of CKD-PD patients while absent from controls. Antibiotic resistance phenotyping revealed mostly putative intrinsic resistance phenotypes (to amoxicillin, ticarcillin, and cephalothin), and resistance to sulfamethoxazole (~43% of isolates) and streptomycin (~17%). However, all isolates were resistant to at least one of the antibiotics tested and multidrug resistance isolates were only found in CKD-PD group (31,6%). Mobile genetic elements and resistance genes were detected in isolates of the species Raoultella ornithinolytica, Klebsiella pneumoniae, Klebsiella oxytoca, Escherichia coli, and Enterobacter asburiae, mostly originated from CKD-PD patients. PD-related infection history revealed that Enterobacteriaceae were responsible for ~8% of peritonitis and ~ 16% of exit-site infections episodes in CKD-PD patients, although no association was found to oral enterobacteria colonization at the time of sampling. The results suggest that the CKD-induced alterations of the oral milieu might promote a dysbiosis of the commensal oral microbiome, namely the proliferation of clinically relevant Enterobacteriaceae potentially harboring acquired antibiotic resistance genes. This study highlights the importance of the oral cavity as a reservoir for pathobionts and antibiotic resistances in CKD patients undergoing peritoneal dialysis.
publishDate 2021
dc.date.none.fl_str_mv 2021-12-14
2021-12-14T00:00:00Z
2022-01-04T15:45:33Z
dc.type.status.fl_str_mv info:eu-repo/semantics/publishedVersion
dc.type.driver.fl_str_mv info:eu-repo/semantics/article
format article
status_str publishedVersion
dc.identifier.uri.fl_str_mv http://hdl.handle.net/10400.14/36349
url http://hdl.handle.net/10400.14/36349
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv 1664-302X
10.3389/fmicb.2021.736685
85121861915
PMC8713742
34970231
000737518800001
dc.rights.driver.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
instname:Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron:RCAAP
instname_str Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
instacron_str RCAAP
institution RCAAP
reponame_str Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
collection Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
repository.name.fl_str_mv Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos) - Agência para a Sociedade do Conhecimento (UMIC) - FCT - Sociedade da Informação
repository.mail.fl_str_mv
_version_ 1799132015888433152