Absence of Shiga toxin-producing Escherichia coli (STEC) in organic leafy greens from the metropolitan region of São Paulo, Brazil.
Leafy greens
Organic vegetables
STEC
Shiga-producing Escherichia coli
Vegetables
Journal
Brazilian journal of microbiology : [publication of the Brazilian Society for Microbiology]
ISSN: 1678-4405
Titre abrégé: Braz J Microbiol
Pays: Brazil
ID NLM: 101095924
Informations de publication
Date de publication:
Sep 2023
Sep 2023
Historique:
received:
01
06
2023
accepted:
12
07
2023
pmc-release:
18
07
2024
medline:
11
9
2023
pubmed:
19
7
2023
entrez:
18
7
2023
Statut:
ppublish
Résumé
Shiga toxin-producing Escherichia coli (STEC) is an important pathogen with public health implications, including its potential association with vegetables. In this study, we investigated the presence of STEC in vegetables obtained from organic producers located in São Paulo city, Brazil. As part of a routine surveillance study conducted over (years of isolation), a total of 200 samples of organic vegetables were screened using biochemical and PCR methods. Among the vegetable samples tested, 30 (15%) were positive for non-Shiga toxin-producing E. coli. While no STEC was detected in the organic vegetables in this study, the presence of non-STEC in vegetables raises concerns about the lack of proper hygiene practices during vegetable handling. This contamination represents a public health risk, particularly considering that these isolates can still be pathogenic, and vegetables are often consumed raw. To address this important issue, continuous monitoring of these farms is recommended to ensure the quality and safety of organic vegetables produced for both domestic consumption and exportation.
Identifiants
pubmed: 37464187
doi: 10.1007/s42770-023-01068-1
pii: 10.1007/s42770-023-01068-1
pmc: PMC10484845
doi:
Substances chimiques
Escherichia coli Proteins
0
Types de publication
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
2253-2258Informations de copyright
© 2023. The Author(s) under exclusive licence to Sociedade Brasileira de Microbiologia.
Références
Hughner R, McDonagh P, Prothero A, Shultz C, Stanton F (2007) Who are organic food consumers? A compilation and review of why people purchase organic food. J Consum Behav 6:94–110
doi: 10.1002/cb.210
Oliveira M, Viñas I, Usall J, Anguera M, Abadias M (2010) Microbiological quality of fresh lettuce from organic and conventional production. Food Microbiol 27:679–684
doi: 10.1016/j.fm.2010.03.008
pubmed: 20510788
Maffei DF, Batalha EY, Landgraf M, Schaffner DW, Franco BDGM (2016) Microbiology of organic and conventionally grown fresch produce. Braz J Microbiol 47S:99–105
doi: 10.1016/j.bjm.2016.10.006
Santos GC, Monteiro M (2004) Sistema Orgânico de produção de alimentos. Aliment Nutr 15:73–86
Doyle MP, Erickson MC (2012) Opportunities for mitigating pathogen contamination during on-farm food production. Int J Food Microbiol 152:54–74
doi: 10.1016/j.ijfoodmicro.2011.02.037
pubmed: 21474196
Abe CM, Matheus-Guimarães C, Garcia BG, Cabilio Guth BE (2020) Interactions of Shiga toxin-producing Escherichia coli with leafy green vegetables. Braz J Microbiol 51(2):797–803
doi: 10.1007/s42770-020-00251-y
pubmed: 32125677
pmcid: 7203381
Lacombe A, Quintela IA, Liao Y-T, Wu VCH (2022) Shiga toxin-producing Escherichia coli outbreaks in California’s leafy greens production continuum. Front Food Sci Technol 2:1068690
doi: 10.3389/frfst.2022.1068690
Bonyadian M, Moshtaghi H, Mohamadtaghipour L (2017) Antibiotic resistance of verotoxigenic Escherichia coli isolated from vegetables. BJM 5:9–16
Kuan C, Rukayadi Y, Ahmad SH, Radzi CWJWM, Thung T, Premarathne JMKJK, Chang W, Loo Y, Tan C, Ramzi OB, Fadzil SNM, Kuan C, Yeo S, Nishibuchi M, Radu S (2017) Comparison of the microbiological quality and safety between conventional and organic vegetables sold in Malaysia. Front Microbiol 8:1433
doi: 10.3389/fmicb.2017.01433
pubmed: 28824567
pmcid: 5534447
Marshall KE, Hexemer A, Seelman SL, Fatica MK, Blessington T, Hajmeer M, Kisselburgh H, Atkinson R, Hill K, Sharma D, Needham M, Peralta V, Higa J, Blickenstaff K, Williams IT, Jhung MA, Wise M, Gieraltowski L (2020) Lessons learned from a decade of investigations of Shiga toxin-producing Escherichia coli outbreaks linked to leafy greens, United States and Canada. Emerg Infect Dis 26(10):2319–2328
doi: 10.3201/eid2610.191418
pubmed: 32946367
pmcid: 7510726
Jenkins C, Dallman TJ, Launders N, Willis C, Byrne L, Jorgensen F, Eppinger M, Adak GK, Aird H, Elviss N, Grant KA, Morgan D, McLauchlin J (2017) Public health investigation of two outbreaks of Shiga toxin-producing Escherichia coli O157 associated with consumption of watercress. Appl Environ Microbiol 81:3946–3952
doi: 10.1128/AEM.04188-14
CDC - Centers for Disease Control and Prevention (2019a) Multistate outbreak of Escherichia coli O157:H7 infections linked to romaine lettuce (Final Update). https://www.cdc.gov/ecoli/2018/o157h7-04-18/index.html . Accessed 23 Jan 2019
CDC - Centers for Disease Control and Prevention (2019b) Outbreak of Escherichia coli infections linked to romaine lettuce. https://www.cdc.gov/ecoli/2018/o157h7-04-18/index.html . Accessed 8 Jan 2019
Pugh HL, Connor C, Siasat P, McNally A, Blair JMA (2023) E. coli ST11 (O157:H7) does not encode a functional AcrF efflux pump. Microbiology 169(4):001324
doi: 10.1099/mic.0.001324
pubmed: 37074150
pmcid: 10202319
Catarame TMG, O´Hanlon KA, Duffy G, Sheridan JJ, Blair IS, DA MD (2003) Optimization of enrichment and plating procedures for the recovery of Escherichia coli O111 and O26 from minced beef. J Appl Microbiol 38:33–43
Toledo MRF, Fontes CF, Trabulsi LR (1982a)) Mili – Um meio para realização dos testes de Motilidade, Indol e Lisina Descarboxilase. Rev Microbiol 13:230–235
Toledo MRF, Fontes CF, Trabulsi LR (1982b)) EPM – Modificação do meio de Rugai e Araújo para a realização simultânea dos testes de produção de gás a partir da glicose, H2S, urease e triptofano desaminase. Rev Microbiol 13:309–315
Feng P, Monday SR (2000) Multiplex PCR for detection of trait and virulence factors in enterohemorrhagic Escherichia coli serotypes. Mol Cell Probes 14:333–337
doi: 10.1006/mcpr.2000.0323
pubmed: 11090262
Paton JC, Paton AW (1998) Patogenesis and diagnosis of Shiga toxin-producing Escherichia coli infections. Clin Microbiol Rev 11:450–479
doi: 10.1128/CMR.11.3.450
pubmed: 9665978
pmcid: 88891
Gannon VP, D'Souza S, Graham T, King RK, Rahn K, Read S (1997) Use of the flagellar H7 gene as a target in multiplex PCR assays and improved specificity in identification of enterohemorrhagic Escherichia coli strains. J Clin Microbiol 35:656–662
doi: 10.1128/jcm.35.3.656-662.1997
pubmed: 9041407
pmcid: 229645
Silva N, Silveira NFA, Yokoya F, Okazadi MM (2003) Ocorrência de Escherichia coli O157:H7 em vegetais e resistência aos agentes de desinfecção em verduras. Ciênc Tecnol Aliment 23:167–173
doi: 10.1590/S0101-20612003000200011
de Quadros Rodrigues R, Loiko MR, de Paula CM, Hessel CT, Jacxsens L, Uyttendaele M, Bender RJ, Tondo EC (2014) Microbiological contamination linked to implementation of good agricultural practices in the production of organic lettuce in Southern Brazil. Food Control 42:152–164
doi: 10.1016/j.foodcont.2014.01.043
Jung Y, Jang H, Matthews KR (2014) Effect of the food production chain from farm practices to vegetable processing on outbreak incidence. Microb Biotechnol 7:517–527
doi: 10.1111/1751-7915.12178
pubmed: 25251466
pmcid: 4265071
Oliveira M, Viñas I, Usall J, Anguera M, Abadias M (2012) Presence and survival of Escherichia coli O157:H7 on lettuce leaves and in soil treated with contaminatd compost and irrigation water. Int J Food Microbiol 156:133–149
doi: 10.1016/j.ijfoodmicro.2012.03.014
pubmed: 22483400
Sapountzis P, Segura A, Desvaux M, Forano E (2020) An overview of the elusive passenger in the gastrointestinal tract of cattle: the Shiga toxin producing Escherichia coli. Microorganisms 8(6):877
doi: 10.3390/microorganisms8060877
pubmed: 32531983
pmcid: 7355788
Sodha SV, Heiman K, Gould LH, Bishop R, Iwamoto M, Swerdlow DL, Griffin PM (2014) National patterns of Escherichia coli O157 infections, USA, 1996-2011. Epidemiol Infect 143:267–273
doi: 10.1017/S0950268814000880
pubmed: 24731294
pmcid: 6542353
Castro VS, Figueiredo EES, Stanford K, McAllister T, Conte-Junior CA (2019) Shiga-toxin producing Escherichia coli in Brazil: a systematic review. Microorganisms 7(5):137
doi: 10.3390/microorganisms7050137
pubmed: 31100803
pmcid: 6560443
Stella AE, Maluta RP, Rigobelo EC, Marin JM, Ávila FA (2012) Virulence genes in isolates of Escherichia coli from samples of milk and feces from dairy cattle. J Food Prot 75:1698–1700
doi: 10.4315/0362-028x.JFP-11-468
pubmed: 22947478
Farah SMSS, De Souza EM, Pedrosa FO, Irino K, Da Silva LR, Rigo LU, Steffens MB, Pigatto CP, Fadel-Picheth CMT (2007) Phenotypic and genotypic traits of Shiga toxin-producing Escherichia coli strains isolated from beef cattle from Paraná State, southern Brazil. Lett Appl Microbiol 44:607–612
doi: 10.1111/j.1472-765X.2007.02123.x
pubmed: 17576221
Vettorato MP, de Castro AF, Cergole-Novella MC, Camargo FL, Irino K, Guth BE (2009) Shiga toxin-producing Escherichia coli and atypical enteropathogenic Escherichia coli strains isolated from healthy sheep of different populations in São Paulo, Brazil. Lett Appl Microbiol 49:53–59
doi: 10.1111/j.1472-765X.2009.02617.x
pubmed: 19413771
Puño-Sarmiento J, Gazal LE, Medeiros LP, Nishio EK, Kobayashi RKT, Nakazato G (2014) Identification of diarrheagenic Escherichia coli strains from avian organic fertilizers. Int J Environ Res Public Health 11:8924–8939
doi: 10.3390/ijerph110908924
pubmed: 25170683
pmcid: 4198998
Wood JL, Chen JC, Elsie F, Delaquis P, Allen KJ (2015) Microbiological survey of locally grown lettuce sold at farmer’s markets in Vancouver, British Columbia. J Food Prot 1:203–208
doi: 10.4315/0362-028X.JFP-14-199
Saeed AY, Mazin H, Saadi AA, Hussein SO (2013) Detection of Escherichia coli O157 in vegetables. IOSR-JAVS 6:16–18
doi: 10.9790/2380-0621618
Loncaveric S, Johannessen GS, Rorvik LM (2005) Bacteriological quality of organically grown leaf lettuce in Norway. Lett Appl Microbiol 41:186–189
doi: 10.1111/j.1472-765X.2005.01730.x
Ryu JH, Kim M, Kim EG, Beuchat LR, Kim H (2014) Comparison of the microbiological quality of environmentally friendly and conventionally grown vegetables sold at retail markets in Korea. J Food Sci 79:M1739–M1744
doi: 10.1111/1750-3841.12531
pubmed: 25124136
Marine SC, Pagadala S, Wang F, Pahl D, Melendez MV, Kline WL, Oni RA, Walsh CS, Everts KL, Buchanan RL, Micallef SA (2015) The growing season, but not the farming system, is a food safety risk determinant for leafy greens in the Mid-Atlantic region of the United States. Appl Environ Microbiol 8:2395–2407
doi: 10.1128/AEM.00051-15
Khalil RKS, Gomaa MAE, Khalil MIM (2015) Detection of Shiga-toxin producing E. coli (STEC) in leafy greens sold at local retail markets in Alexandria, Egypt. Int J Food Microbiol 197:58–64
doi: 10.1016/j.ijfoodmicro.2014.12.019
pubmed: 25557184
Mazaheri S, Ahrabi SS, Aslani MM (2014) Shiga-toxin producing Escherichia coli isolated from lettuce samples in Tehran, Iran. Jundishapur J. Microbiol 7:e12346
doi: 10.5812/jjm.12346
pubmed: 25774272
pmcid: 4332234
Özpinar H, Turan B, Tekiner IH, Tezmen G, Gökçe I, Akineden Ö (2013) Evaluation of pathogenic Escherichia coli occurrence in vegetable samples from district bazaars in Istanbul using real-time PCR. Lett Appl Microbiol 57:362–367
doi: 10.1111/lam.12122
pubmed: 23789811
Pinaka O, Pournaras S, Mouchtouri V, Plakokefalos E, Katsiaflaka A, Kolokythopoulou F, Barboutsi E, Bitsolas N, Hadjichristodoulou C (2013) Shiga-toxin producing Escherichia coli in Central Greece: prevalence and virulence genes of O157:H7 and non-O157 in animal feces, vegetables and humans. Eur J Clin Microbiol Infect Dis 32:1401–1408
doi: 10.1007/s10096-013-1889-6
pubmed: 23677425
Lenzi A, Marvasi M, Baldi A (2021) Agronomic practices to limit pre-and post-harvest contamination and proliferation of human pathogenic Enterobacteriaceae in vegetable produce. Food Control 119:107486
doi: 10.1016/j.foodcont.2020.107486