Ruminant-associated Listeria monocytogenes isolates belong preferentially to dairy-associated hypervirulent clones: a longitudinal study in 19 farms.
Journal
Environmental microbiology
ISSN: 1462-2920
Titre abrégé: Environ Microbiol
Pays: England
ID NLM: 100883692
Informations de publication
Date de publication:
12 2021
12 2021
Historique:
received:
03
08
2021
accepted:
24
11
2021
pubmed:
5
12
2021
medline:
18
3
2022
entrez:
4
12
2021
Statut:
ppublish
Résumé
Studies have shown that ruminants constitute reservoirs of Listeria monocytogenes, but little is known about the epidemiology and genetic diversity of this pathogen within farms. Here we conducted a large-scale longitudinal study to monitor Listeria spp. in 19 dairy farms during three consecutive seasons (N = 3251 samples). L. innocua was the most prevalent species, followed by L. monocytogenes. Listeria monocytogenes was detected in 52.6% of farms and more frequently in cattle (4.1%) and sheep (4.5%) than in goat farms (0.2%). Lineage I accounted for 69% of L. monocytogenes isolates. Among animal samples, the most prevalent sublineages (SL) and clonal complexes (CC) were SL1/CC1, SL219/CC4, SL26/CC26 and SL87/CC87, whereas SL666/CC666 was most prevalent in environmental samples. Sixty-one different L. monocytogenes cgMLST types were found, 28% common to different animals and/or surfaces within the same farm and 21% previously reported elsewhere in the context of food and human surveillance. Listeria monocytogenes prevalence was not affected by farm hygiene but by season: higher prevalence was observed during winter in cattle, and during winter and spring in sheep farms. Cows in their second lactation had a higher probability of L. monocytogenes faecal shedding. This study highlights dairy farms as a reservoir for hypervirulent L. monocytogenes.
Identifiants
pubmed: 34863016
doi: 10.1111/1462-2920.15860
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
7617-7631Informations de copyright
© 2021 The Authors. Environmental Microbiology published by Society for Applied Microbiology and John Wiley & Sons Ltd.
Références
Addis, M.F., Cubeddu, T., Pilicchi, Y., Rocca, S., and Piccinini, R. (2019) Chronic intramammary infection by Listeria monocytogenes in a clinically healthy goat - a case report. BMC Vet Res 15: 229.
Borucki, M.K., Gay, C.C., Reynolds, J., McElwain, K.L., Kim, S.H., Call, D.R., and Knowles, D.P. (2005) Genetic diversity of Listeria monocytogenes strains from a high-prevalence dairy farm. Appl Environ Microbiol 71: 5893-5899.
Carlin, C.R., Liao, J., Weller, D., Guo, X., Orsi, R., and Wiedmann, M. (2021) Listeria cossartiae sp. nov., Listeria immobilis sp. nov., Listeria portnoyi sp. nov. and Listeria rustica sp. nov., isolated from agricultural water and natural environments. Int J Syst Evol Microbiol 71: 004795.
Castro, H., Jaakkonen, A., Hakkinen, M., Korkeala, H., and Lindström, M. (2018) Occurrence, persistence, and contamination routes of Listeria monocytogenes genotypes on three Finnish dairy cattle farms: a longitudinal study. Appl Environ Microbiol 84: 1-14.
Cavicchioli, R., Ripple, W.J., Timmis, K.N., Azam, F., Bakken, L.R., Baylis, M., et al. (2019) Scientists' warning to humanity: microorganisms and climate change. Nat Rev Microbiol 17: 569-586.
Charlier, C., Perrodeau, É., Leclercq, A., Cazenave, B., Pilmis, B., Henry, B., et al. (2017) Clinical features and prognostic factors of listeriosis: the MONALISA national prospective cohort study. Lancet Infect Dis 17: 510-519.
Chow, J.T.H., Gall, A.R., Johnson, A.K., and Huynh, T.N. (2021) Characterization of Listeria monocytogenes isolates from lactating dairy cows in a Wisconsin farm: antibiotic resistance, mammalian cell infection, and effects on the fecal microbiota. J Dairy Sci 104: 4561-4574.
Clinical and Laboratory Standards Institute (CLSI) (2017) Performance standards for antimicrobial susceptibility testing - approved guideline M100, 27th ed.
Cooper, J., and Walker, R.D. (1998) Listeriosis. Vet Clin North Am Food Anim Pract 14: 113-125.
Costard, S., Espejo, L., Groenendaal, H., and Zagmutt, F.J. (2017) Outbreak-related disease burden associated with consumption of unpasteurized cow's milk and cheese, United States, 2009-2014. Emerg Infect Dis 23: 957-964.
Dell'Armelina Rocha, P.R., Lomonaco, S., Bottero, M.T., Dalmasso, A., Dondo, A., Grattarola, C., et al. (2013) Ruminant rhombencephalitis-associated Listeria monocytogenes strains constitute a genetically homogeneous group related to human outbreak strains. Appl Environ Microbiol 79: 3059-3066.
Doumith, M., Buchrieser, C., Glaser, P., Jacquet, C., and Martin, P. (2004) Differentiation of the major Listeria monocytogenes Serovars by multiplex PCR. J Clin Microbiol 42: 3819-3822.
Dreyer, M., Aguilar-Bultet, L., Rupp, S., Guldimann, C., Stephan, R., Schock, A., et al. (2016) Listeria monocytogenes sequence type 1 is predominant in ruminant rhombencephalitis. Sci Rep 6: 36419.
Esteban, J.I., Oporto, B., Aduriz, G., Juste, R.A., and Hurtado, A. (2009) Faecal shedding and strain diversity of Listeria monocytogenes in healthy ruminants and swine in northern Spain. BMC Vet Res 5: 1-10.
EUCAST. (2020) Disk diffusion method for antimicrobial susceptibility testing, version 9.
European Union. (2010) Directive 2010/63/EU of the European Parliament and of the Council of 22 September 2010 on the protection of animals used for scientific purposes. Off J Eur Union: 33-79.
Fox, E., Hunt, K., O'Brien, M., and Jordan, K. (2011) Listeria monocytogenes in Irish Farmhouse cheese processing environments. Int J Food Microbiol 145: S39-S45.
Gray, M.J., Zadoks, R.N., Fortes, E.D., Dogan, B., Cai, S., Chen, Y., et al. (2004) Listeria monocytogenes isolates from foods and humans form distinct but overlapping populations. Appl Environ Microbiol 70: 5833-5841.
Grif, K., Patscheider, G., Dierich, M.P., and Allerberger, F. (2003) Incidence of fecal carriage of Listeria monocytogenes in three healthy volunteers: a one-year prospective stool survey. Eur J Clin Microbiol Infect Dis 22: 16-20.
Hafner, L., Pichon, M., Burucoa, C., Nusser, S.H., Moura, A., Garcia-Garcera, M., and Lecuit, M. (2021) Listeria monocytogenes faecal carriage is common and depends on the gut microbiota. Nat Commun 12: 6826.
Haley, B.J., Sonnier, J., Schukken, Y.H., Karns, J.S., and Van Kessel, J.A.S. (2015) Diversity of Listeria monocytogenes within a U.S. Dairy Herd, 2004-2010. Foodborne Pathog Dis 12: 844-850.
Ho, A.J., Ivanek, R., Gröhn, Y.T., Nightingale, K.K., and Wiedmann, M. (2007) Listeria monocytogenes fecal shedding in dairy cattle shows high levels of day-to-day variation and includes outbreaks and sporadic cases of shedding of specific L. monocytogenes subtypes. Prev Vet Med 80: 287-305.
Hurley, D., Luque-Sastre, L., Craig, T.P., Huynh, S., Eshwar, A.K., Nguyen, S.V., et al. (2019) Whole-genome sequencing-based characterization of 100 Listeria monocytogenes isolates collected from food processing environments over a four-year period. mSphere 4: e00252-19.
Hurtado, A., Ocejo, M., and Oporto, B. (2017) Salmonella spp. and Listeria monocytogenes shedding in domestic ruminants and characterization of potentially pathogenic strains. Vet Microbiol 210: 71-76.
Husu, J.R. (1990) Epidemiological studies on the occurrence of Listeria monocytogenes in the feces of dairy cattle. J Vet Med Ser B 37: 276-282.
Husu, J.R., Seppänen, J.T., Sivelä, S.K., and Rauramaa, A.L. (1990) Contamination of raw Milk by Listeria monocytogenes on dairy farms. J Vet Med Ser B 37: 268-275.
Hutcheson, K. (1970) A test for comparing diversities based on the shannon formula. J Theor Biol 29: 151-154.
Ianevski, A., Zusinaite, E., Shtaida, N., Kallio-Kokko, H., Valkonen, M., Kantele, A., et al. (2019) Low temperature and low UV indexes correlated with peaks of influenza virus activity in northern Europe during 2010-2018. Viruses 11: 207.
Jayarao, B.M., Donaldson, S.C., Straley, B.A., Sawant, A.A., Hegde, N.V., and Brown, J.L. (2006) A survey of foodborne pathogens in bulk tank milk and raw milk consumption among farm families in Pennsylvania. J Dairy Sci 89: 2451-2458.
Jolley, K.A., and Maiden, M.C.J. (2010) BIGSdb: scalable analysis of bacterial genome variation at the population level. BMC Bioinformatics 11: 595.
Keys, A.L., Dailey, R.C., Hitchins, A.D., and Smiley, R.D. (2013) Postenrichment population differentials using buffered Listeria enrichment broth: implications of the presence of Listeria innocua on Listeria monocytogenes in food test samples. J Food Prot 76: 1854-1862.
Kwong, J.C., Mercoulia, K., Tomita, T., Easton, M., Li, H.Y., Bulach, D.M., et al. (2016) Prospective whole-genome sequencing enhances national surveillance of listeria monocytogenes. J Clin Microbiol 54: 333-342.
Latorre, A.A., Pradhan, A.K., Van Kessel, J.A.S., Karns, J.S., Boor, K.J., Rice, D.H., et al. (2011) Quantitative risk assessment of listeriosis due to consumption of raw milk. J Food Prot 74: 1268-1281.
Latorre, A.A., Van Kessel, J.S., Karns, J.S., Zurakowski, M.J., Pradhan, A.K., Boor, K.J., et al. (2010) Biofilm in milking equipment on a dairy farm as a potential source of bulk tank milk contamination with Listeria monocytogenes. J Dairy Sci 93: 2792-2802.
Letunic, I., and Bork, P. (2021) Interactive tree of life (iTOL) v5: an online tool for phylogenetic tree display and annotation. Nucleic Acids Res 49: W293-W296.
Linnan, M.J., Mascola, L., Lou, X.D., Goulet, V., May, S., Salminen, C., et al. (1988) Epidemic listeriosis associated with Mexican-style cheese. N Engl J Med 319: 823-828.
MacDonald, P.D.M., Whitwam, R.E., Boggs, J.D., MacCormack, J.N., Anderson, K.L., Reardon, J.W., et al. (2005) Outbreak of listeriosis among Mexican immigrants as a result of consumption of illicitly produced Mexican-style cheese. Clin Infect Dis 40: 677-682.
Maury, M.M., Bracq-Dieye, H., Huang, L., Vales, G., Lavina, M., Thouvenot, P., et al. (2019) Hypervirulent Listeria monocytogenes clones' adaption to mammalian gut accounts for their association with dairy products. Nat Commun 10: 2488.
Maury, M.M., Tsai, Y.H., Charlier, C., Touchon, M., Chenal-Francisque, V., Leclercq, A., et al. (2016) Uncovering Listeria monocytogenes hypervirulence by harnessing its biodiversity. Nat Genet 48: 308-313.
Mohammed, H.O., Stipetic, K., McDonough, P.L., Gonzalez, R.N., Nydam, D.V., and Atwill, E.R. (2009) Identification of potential on-farm sources of Listeria monocytogenes in herds of dairy cattle. Am J Vet Res 70: 383-388.
Moura, A., Criscuolo, A., Pouseele, H., Maury, M.M., Leclercq, A., Tarr, C., et al. (2016) Whole genome-based population biology and epidemiological surveillance of Listeria monocytogenes. Nat Microbiol 2: 16185.
Moura, A., Lefrancq, N., Wirth, T., Leclercq, A., Borges, V., Gilpin, B., et al. (2021) Emergence and global spread of Listeria monocytogenes main clinical clonal complex. Sci Adv 7. https://pubmed.ncbi.nlm.nih.gov/34851675/
Moura, A., Tourdjman, M., Leclercq, A., Hamelin, E., Laurent, E., Fredriksen, N., et al. (2017) Real-time whole-genome sequencing for surveillance of Listeria monocytogenes, France. Emerg Infect Dis 23: 1462-1470.
Murinda, S.E., Nguyen, L.T., Nam, H.M., Almeida, R.A., Headrick, S.J., and Oliver, S.P. (2004) Detection of sorbitol-negative and sorbitol-positive Shiga toxin-producing Escherichia coli, Listeria monocytogenes, Campylobacter jejuni, and Salmonella spp. in dairy farm environmental samples. Foodborne Pathog Dis 1: 97-104.
Nightingale, K.K., Schukken, Y.H., Nightingale, C.R., Fortes, E.D., Ho, A.J., Her, Z., et al. (2004) Ecology and transmission of Listena monocytogenes infecting ruminants and in the farm environment. Appl Environ Microbiol 70: 4458-4467.
Oliver, S.P., Jayarao, B.M., and Almeida, R.A. (2005) Foodborne pathogens in milk and the dairy farm environment: food safety and public health implications. Foodborne Pathog Dis 2: 115-129.
Orsi, R.H., and Wiedmann, M. (2016) Characteristics and distribution of Listeria spp., including Listeria species newly described since 2009. Appl Microbiol Biotechnol 100: 5273-5287.
Painset, A., Björkman, J.T., Kiil, K., Guillier, L., Mariet, J.-F., Félix, B., et al. (2019) LiSEQ - whole-genome sequencing of a cross-sectional survey of Listeria monocytogenes in ready-to-eat foods and human clinical cases in Europe. Microb Genomics 5: e000257.
Palacios-Gorba, C., Moura, A., Leclercq, A., Gómez-Martín, Á., Gomis, J., Jiménez-Trigos, E., et al. (2021) Listeria spp. isolated from tonsils of wild deer and boars: genomic characterization. Appl Environ Microbiol 87: e02651-20.
Papić, B., Pate, M., Félix, B., and Kušar, D. (2019) Genetic diversity of Listeria monocytogenes strains in ruminant abortion and rhombencephalitis cases in comparison with the natural environment. BMC Microbiol 19: 299.
Pérez-Trallero, E., Zigorraga, C., Artieda, J., Alkorta, M., and Marimón, J.M. (2014) Two outbreaks of Listeria monocytogenes infection, northern Spain. Emerg Infect Dis 20: 2155-2157.
Prjibelski, A., Antipov, D., Meleshko, D., Lapidus, A., and Korobeynikov, A. (2020) Using SPAdes de novo assembler. Curr Protoc Bioinformatics 70: e102.
Quereda, J.J., Leclercq, A., Moura, A., Vales, G., Gómez-Martín, Á., García-Muñoz, Á., et al. (2020) Listeria valentina sp. nov., isolated from a water trough and the faeces of healthy sheep. Int J Syst Evol Microbiol 70: 5868-5879.
Ragon, M., Wirth, T., Hollandt, F., Lavenir, R., Lecuit, M., Le Monnier, A., and Brisse, S. (2008) A new perspective on Listeria monocytogenes evolution. PLoS Pathog 4: e1000146.
Ramage, C.P., Low, J.C., McLauchlin, J., and Donachie, W. (1999) Characterisation of listeria ivanovii isolates from the UKusing pulsed-field gel electrophoresis. FEMS Microbiol Lett 170: 349-353.
Reneau, J.K., Seykora, A.J., Heins, B.J., Endres, M.I., Farnsworth, R.J., and Bey, R.F. (2005) Association between hygiene scores and somatic cell scores in dairy cattle. J Am Vet Med Assoc 227: 1297-1301.
Robertson, J., and Nash, J.H.E. (2018) MOB-suite: software tools for clustering, reconstruction and typing of plasmids from draft assemblies. Microb Genomics 4: e000206.
Roche, J.R., Friggens, N.C., Kay, J.K., Fisher, M.W., Stafford, K.J., and Berry, D.P. (2009) Invited review: body condition score and its association with dairy cow productivity, health, and welfare. J Dairy Sci 92: 5769-5801.
Sanaa, M., Poutrel, B., Menard, J.L., and Serieys, F. (1993) Risk factors associated with contamination of raw milk by Listeria monocytogenes in dairy farms. J Dairy Sci 76: 2891-2898.
Sauders, B.D., Overdevest, J., Fortes, E., Windham, K., Schukken, Y., Lembo, A., and Wiedmann, M. (2012) Diversity of Listeria species in urban and natural environments. Appl Environ Microbiol 78: 4420-4433.
Schlech, W.F., Lavigne, P.M., Bortolussi, R.A., Allen, A.C., Haldane, E.V., Wort, A.J., et al. (1983) Epidemic listeriosis - evidence for transmission by food. N Engl J Med 308: 203-206.
Skovgaard, N., and Morgen, C.A. (1988) Detection of Listeria spp. in faeces from animals, in feeds, and in raw foods of animal origin. Int J Food Microbiol 6: 229-242.
Stasiewicz, M.J., Oliver, H.F., Wiedmann, M., and den Bakker, H.C. (2015) Whole-genome sequencing allows for improved identification of persistent Listeria monocytogenes in food-associated environments. Appl Environ Microbiol 81: 6024-6037.
Swaminathan, B., and Gerner-Smidt, P. (2007) The epidemiology of human listeriosis. Microbes Infect 9: 1236-1243.
Thouvenot, P., Vales, G., Bracq-Dieye, H., Tessaud-Rita, N., Maury, M.M., Moura, A., et al. (2018) MALDI-TOF mass spectrometry-based identification of Listeria species in surveillance: a prospective study. J Microbiol Methods 144: 29-32.
Van Kessel, J.A.S., Karns, J.S., Lombard, J.E., and Kopral, C.A. (2011) Prevalence of Salmonella enterica, Listeria monocytogenes, and Escherichia coli virulence factors in bulk tank milk and in-line filters from U.S. dairies. J Food Prot 74: 759-768.
Vázquez-Boland, J.A., Kuhn, M., Berche, P., Chakraborty, T., Domı́nguez-Bernal, G., Goebel, W., et al. (2001) Listeria pathogenesis and molecular virulence determinants. Clin Microbiol Rev 14: 584-640.
Vilar, M.J., Yus, E., Sanjuán, M.L., Diéguez, F.J., and Rodríguez-Otero, J.L. (2007) Prevalence of and risk factors for Listeria species on dairy farms. J Dairy Sci 90: 5083-5088.
Walland, J., Lauper, J., Frey, J., Imhof, R., Stephan, R., Seuberlich, T., and Oevermann, A. (2015) Listeria monocytogenes infection in ruminants: is there a link to the environment, food and human health? A review. Schweiz Arch Tierheilkd 157: 319-328.
Wang, H., Luo, L., Zhang, Z., Deng, J., Wang, Y., Miao, Y., et al. (2018) Prevalence and molecular characteristics of Listeria monocytogenes in cooked products and its comparison with isolates from listeriosis cases. Front Med 12: 104-112.
Wiedmann, M., Bruce, J.L., Keating, C., Johnson, A.E., McDonough, P.L., and Batt, C.A. (1997) Ribotypes and virulence gene polymorphisms suggest three distinct Listeria monocytogenes lineages with differences in pathogenic potential. Infect Immun 65: 2707-2716.
Winter, P., Schilcher, F., Bagò, Z., Schoder, D., Egerbacher, M., Baumgartner, W., and Wagner, M. (2004) Clinical and histopathological aspects of naturally occurring mastitis caused by Listeria monocytogenes in cattle and ewes. J Vet Med Ser B Infect Dis Vet Public Heal 51: 176-179.
Yusuf, S., Piedimonte, G., Auais, A., Demmler, G., Krishnan, S., Van Caeseele, P., et al. (2007) The relationship of meteorological conditions to the epidemic activity of respiratory syncytial virus. Epidemiol Infect 135: 1077-1090.
Zhang, H., Chen, W., Wang, J., Xu, B., Liu, H., Dong, Q., and Zhang, X. (2020) 10-year molecular surveillance of Listeria monocytogenes using whole-genome sequencing in Shanghai, China, 2009-2019. Front Microbiol 11: 551020.
Zhao, Q., Hu, P., Li, Q., Zhang, S., Li, H., Chang, J., et al. (2021) Prevalence and transmission characteristics of Listeria species from ruminants in farm and slaughtering environments in China. Emerg Microbes Infect 10: 356-364.
Zundel, E., and Bernard, S. (2006) Listeria monocytogenes translocates throughout the digestive tract in asymptomatic sheep. J Med Microbiol 55: 1717-1723.