Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal

Detalhes bibliográficos
Autor(a) principal: Oliveira, Ricardo
Data de Publicação: 2022
Outros Autores: Pinho, Eva, Almeida, Gonçalo, Azevedo, Nuno F., Almeida, Carina Manuela Fernandes
Tipo de documento: Artigo
Idioma: eng
Título da fonte: Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
Texto Completo: https://hdl.handle.net/1822/76689
Resumo: Staphylococcus aureus and staphylococcal enterotoxins are a serious public health concern associated with hospital and community-acquired illnesses. Dairy animals frequently shed S. aureus into the milk supply which can lead to food poisoning in humans. This study aims to investigate the prevalence and genetic diversity of S. aureus and staphylococcal enterotoxins in raw milk from the main dairy region of mainland Portugal. S. aureus was found in 53.0% (95% CI: 40.665.4%) of 100 raw cows milk samples collected from bulk cooling tanks. The highest contamination level was 3.4 log10 CFU.mL<sup>1</sup>, and in some samples more than one S. aureus strain was identified. Staphylococcal enterotoxins (SEA-SEE) were detected in one sample. Spa typing revealed 62 distinct S. aureus isolates, being t529 (17.7%, 95% CI: 8.227.3%) and t1403 (16.1%, 95% CI: 7.025.3%) the predominant types, commonly associated with livestock infection or carriage. The antimicrobial susceptibility test showed that 35.5% of the S. aureus isolates were resistant to at least one antimicrobial agent, with resistance to penicillin being the highest (32.3%, 95% CI: 20.643.9%) followed by tetracycline (24.2%, 95% CI: 13.534.9%), ciprofloxacin (16.1%, 95% CI: 7.025.3%) and chloramphenicol (16.1%, 95% CI: 7.025.3%). Moreover, five isolates (8.1%, 95% CI: 1.314.8%) were identified as methicillin-resistant S. aureus (MRSA, cefoxitin resistant). Regarding virulence/resistance genes, 46,8% (95% CI: 34.459.2%) isolates harbored at least one enterotoxin-encoding gene, and the seg gene was the most frequently detected (41.9%, 95% CI: 29.754.2%) followed by the sei (40.3%, 95% CI: 28.152.5%), sec (6.5%, 95% CI: 0.312.6%), seh (4.8%, 95% CI: 0.010.2%), and sea (1.6%, 95% CI: 0.04.7%) genes. Five (8.1%, 95% CI: 1.314.8%) non-enterotoxigenic isolates carried the mecA gene (corresponding to isolates phenotypically classified as MRSA), and 4.8% (95% CI: 0.010.2%) enterotoxigenic strains also had the tsst-1 gene. Our study confirm that raw milk can be a zoonotic source of S. aureus, including enterotoxigenic and MRSA strains. Furthermore, the majority of enterotoxigenic isolates were found to contain genes encoding SEs (SEG, SEH and SEI) not routinely screened. This shows the need for a broader SE screening in food safety control, as well as the relevance of risk mitigation measures to control S. aureus transmission along the food chain in Portugal.
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spelling Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern PortugalStaphylococcus aureusRaw milkStaphylococcal enterotoxinsMRSASpa typingScience & TechnologyStaphylococcus aureus and staphylococcal enterotoxins are a serious public health concern associated with hospital and community-acquired illnesses. Dairy animals frequently shed S. aureus into the milk supply which can lead to food poisoning in humans. This study aims to investigate the prevalence and genetic diversity of S. aureus and staphylococcal enterotoxins in raw milk from the main dairy region of mainland Portugal. S. aureus was found in 53.0% (95% CI: 40.665.4%) of 100 raw cows milk samples collected from bulk cooling tanks. The highest contamination level was 3.4 log10 CFU.mL<sup>1</sup>, and in some samples more than one S. aureus strain was identified. Staphylococcal enterotoxins (SEA-SEE) were detected in one sample. Spa typing revealed 62 distinct S. aureus isolates, being t529 (17.7%, 95% CI: 8.227.3%) and t1403 (16.1%, 95% CI: 7.025.3%) the predominant types, commonly associated with livestock infection or carriage. The antimicrobial susceptibility test showed that 35.5% of the S. aureus isolates were resistant to at least one antimicrobial agent, with resistance to penicillin being the highest (32.3%, 95% CI: 20.643.9%) followed by tetracycline (24.2%, 95% CI: 13.534.9%), ciprofloxacin (16.1%, 95% CI: 7.025.3%) and chloramphenicol (16.1%, 95% CI: 7.025.3%). Moreover, five isolates (8.1%, 95% CI: 1.314.8%) were identified as methicillin-resistant S. aureus (MRSA, cefoxitin resistant). Regarding virulence/resistance genes, 46,8% (95% CI: 34.459.2%) isolates harbored at least one enterotoxin-encoding gene, and the seg gene was the most frequently detected (41.9%, 95% CI: 29.754.2%) followed by the sei (40.3%, 95% CI: 28.152.5%), sec (6.5%, 95% CI: 0.312.6%), seh (4.8%, 95% CI: 0.010.2%), and sea (1.6%, 95% CI: 0.04.7%) genes. Five (8.1%, 95% CI: 1.314.8%) non-enterotoxigenic isolates carried the mecA gene (corresponding to isolates phenotypically classified as MRSA), and 4.8% (95% CI: 0.010.2%) enterotoxigenic strains also had the tsst-1 gene. Our study confirm that raw milk can be a zoonotic source of S. aureus, including enterotoxigenic and MRSA strains. Furthermore, the majority of enterotoxigenic isolates were found to contain genes encoding SEs (SEG, SEH and SEI) not routinely screened. This shows the need for a broader SE screening in food safety control, as well as the relevance of risk mitigation measures to control S. aureus transmission along the food chain in Portugal.This work was financially supported by LA/P/0045/2020 (ALiCE), UIDB/00511/2020 and UIDP/00511/2020 (LEPABE), funded by national funds through FCT/MCTES (PIDDAC); Project POCI-01-0145-FEDER-028659, funded by FEDER funds through COMPETE2020 – Programa Operacional Competitividade e Internacionalização (POCI); and by national funds (PIDDAC) through FCT/MCTES. The authors also thank FCT for the Ph.D. Fellowship SFRH/BD/138883/2018.info:eu-repo/semantics/publishedVersionFrontiers MediaUniversidade do MinhoOliveira, RicardoPinho, EvaAlmeida, GonçaloAzevedo, Nuno F.Almeida, Carina Manuela Fernandes2022-03-222022-03-22T00:00:00Zinfo:eu-repo/semantics/publishedVersioninfo:eu-repo/semantics/articleapplication/pdfhttps://hdl.handle.net/1822/76689engOliveira, Ricardo; Pinho, Eva; Almeida, Gonçalo; Azevedo, Nuno F.; Almeida, Carina, Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal. Frontiers in Microbiology, 13(846653), 20221664-302X10.3389/fmicb.2022.846653http://journal.frontiersin.org/journal/microbiologyinfo: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:RCAAP2023-07-21T11:57:46Zoai:repositorium.sdum.uminho.pt:1822/76689Portal AgregadorONGhttps://www.rcaap.pt/oai/openaireopendoar:71602024-03-19T18:47:27.516010Repositório 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 Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
title Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
spellingShingle Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
Oliveira, Ricardo
Staphylococcus aureus
Raw milk
Staphylococcal enterotoxins
MRSA
Spa typing
Science & Technology
title_short Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
title_full Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
title_fullStr Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
title_full_unstemmed Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
title_sort Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal
author Oliveira, Ricardo
author_facet Oliveira, Ricardo
Pinho, Eva
Almeida, Gonçalo
Azevedo, Nuno F.
Almeida, Carina Manuela Fernandes
author_role author
author2 Pinho, Eva
Almeida, Gonçalo
Azevedo, Nuno F.
Almeida, Carina Manuela Fernandes
author2_role author
author
author
author
dc.contributor.none.fl_str_mv Universidade do Minho
dc.contributor.author.fl_str_mv Oliveira, Ricardo
Pinho, Eva
Almeida, Gonçalo
Azevedo, Nuno F.
Almeida, Carina Manuela Fernandes
dc.subject.por.fl_str_mv Staphylococcus aureus
Raw milk
Staphylococcal enterotoxins
MRSA
Spa typing
Science & Technology
topic Staphylococcus aureus
Raw milk
Staphylococcal enterotoxins
MRSA
Spa typing
Science & Technology
description Staphylococcus aureus and staphylococcal enterotoxins are a serious public health concern associated with hospital and community-acquired illnesses. Dairy animals frequently shed S. aureus into the milk supply which can lead to food poisoning in humans. This study aims to investigate the prevalence and genetic diversity of S. aureus and staphylococcal enterotoxins in raw milk from the main dairy region of mainland Portugal. S. aureus was found in 53.0% (95% CI: 40.665.4%) of 100 raw cows milk samples collected from bulk cooling tanks. The highest contamination level was 3.4 log10 CFU.mL<sup>1</sup>, and in some samples more than one S. aureus strain was identified. Staphylococcal enterotoxins (SEA-SEE) were detected in one sample. Spa typing revealed 62 distinct S. aureus isolates, being t529 (17.7%, 95% CI: 8.227.3%) and t1403 (16.1%, 95% CI: 7.025.3%) the predominant types, commonly associated with livestock infection or carriage. The antimicrobial susceptibility test showed that 35.5% of the S. aureus isolates were resistant to at least one antimicrobial agent, with resistance to penicillin being the highest (32.3%, 95% CI: 20.643.9%) followed by tetracycline (24.2%, 95% CI: 13.534.9%), ciprofloxacin (16.1%, 95% CI: 7.025.3%) and chloramphenicol (16.1%, 95% CI: 7.025.3%). Moreover, five isolates (8.1%, 95% CI: 1.314.8%) were identified as methicillin-resistant S. aureus (MRSA, cefoxitin resistant). Regarding virulence/resistance genes, 46,8% (95% CI: 34.459.2%) isolates harbored at least one enterotoxin-encoding gene, and the seg gene was the most frequently detected (41.9%, 95% CI: 29.754.2%) followed by the sei (40.3%, 95% CI: 28.152.5%), sec (6.5%, 95% CI: 0.312.6%), seh (4.8%, 95% CI: 0.010.2%), and sea (1.6%, 95% CI: 0.04.7%) genes. Five (8.1%, 95% CI: 1.314.8%) non-enterotoxigenic isolates carried the mecA gene (corresponding to isolates phenotypically classified as MRSA), and 4.8% (95% CI: 0.010.2%) enterotoxigenic strains also had the tsst-1 gene. Our study confirm that raw milk can be a zoonotic source of S. aureus, including enterotoxigenic and MRSA strains. Furthermore, the majority of enterotoxigenic isolates were found to contain genes encoding SEs (SEG, SEH and SEI) not routinely screened. This shows the need for a broader SE screening in food safety control, as well as the relevance of risk mitigation measures to control S. aureus transmission along the food chain in Portugal.
publishDate 2022
dc.date.none.fl_str_mv 2022-03-22
2022-03-22T00:00:00Z
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 https://hdl.handle.net/1822/76689
url https://hdl.handle.net/1822/76689
dc.language.iso.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv Oliveira, Ricardo; Pinho, Eva; Almeida, Gonçalo; Azevedo, Nuno F.; Almeida, Carina, Prevalence and diversity of Staphylococcus aureus and Staphylococcal enterotoxins in raw milk from Northern Portugal. Frontiers in Microbiology, 13(846653), 2022
1664-302X
10.3389/fmicb.2022.846653
http://journal.frontiersin.org/journal/microbiology
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.publisher.none.fl_str_mv Frontiers Media
publisher.none.fl_str_mv Frontiers Media
dc.source.none.fl_str_mv reponame:Repositório Científico de Acesso Aberto de Portugal (Repositórios Cientìficos)
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