Prevalence of bovine mastitis-related pathogens, identified by mass spectrometry in flies (Insecta, Diptera) captured in the milking environment.


Journal

Letters in applied microbiology
ISSN: 1472-765X
Titre abrégé: Lett Appl Microbiol
Pays: England
ID NLM: 8510094

Informations de publication

Date de publication:
Nov 2022
Historique:
revised: 27 06 2022
received: 10 05 2022
accepted: 12 07 2022
pubmed: 25 7 2022
medline: 26 10 2022
entrez: 24 7 2022
Statut: ppublish

Résumé

Diptera (Insecta) are able to transmit approximately 200 pathogenic microorganisms to humans and animals, causing more than 65 diseases, including bovine mastitis, which constitutes a major cause of economic losses in the dairy industry. In this scenario, 217 adult specimens of Diptera were collected from nine farms and identified to the family and/or species level. Of the 11 families recorded, Muscidae was the most prevalent (152 out of 217; 70%). All Diptera specimens were subjected to microbiological culture using conventional and selective media, and isolates were then identified at the species level by mass spectrometry. In total, 275 microorganisms were identified, with a predominance of pathogens related to environmental bovine mastitis (166/275 = 60·4%), that is, Enterococcus species (70/275 = 25·4%) and Escherichia coli (49/275 = 17·8%). Nontraditional agents related to bovine mastitis (called miscellaneous) were detected in 28% (77/275), as well as microorganisms with well-known zoonotic behaviour (e.g. Bacillus cereus). This is study contributes with knowledge of diversity of microorganisms carried by Diptera in the dairy environment, including pathogens associated with environmental and contagious bovine mastitis, and agents with human relevance. To our knowledge, a three-part chromogenic selective medium used to microbial culture of milk on farms was used for the first time to identification of pathogens in Diptera.

Identifiants

pubmed: 35871465
doi: 10.1111/lam.13791
doi:

Types de publication

Journal Article Review

Langues

eng

Sous-ensembles de citation

IM

Pagination

1232-1245

Subventions

Organisme : (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq
ID : #308832/2020-5
Organisme : (Conselho Nacional de Desenvolvimento Científico e Tecnológico, CNPq
ID : #310345/2020-0
Organisme : Fundação de Amparo à Pesquisa do Estado de São Paulo - FAPESP
ID : 2015/19688-8

Informations de copyright

© 2022 Society for Applied Microbiology.

Références

Abera, B., Lemma, D. and Iticha, Y. (2013) Study of bovine mastites in Asella government dairy farm of Oromia regional state. Sout East Ethiop 1, 134-145.
Akdouche, L., Aissi, M. and Saadi, A.J. (2018) Prevalence and identification of yeasts responsible for mastitis in dairy cattle farms in the Sidi Lahcene region in the Wilaya of Sidi bel abbes Algeria. Adv Dairy Res 6, 2.
Akhtar, M., Hirt, H. and Zurek, L. (2009) Horizontal transfer of the tetracycline resistance gene tetM mediated by pCF10 among Enterococcus faecalis in the house Fly (Musca domestica L.) Alimentary Canal. Microb Ecol 58, 509-518.
Ali, S., Alam, M., Hasan, G.M. and Md Hassan, I. (2022) Potential therapeutic targets of Klebsiella pneumoniae: a multi-omics review perspective. Brief Funct Genom 21, 63-77.
Almeida, J.L., Giuffrida, R., Andrade, R.A.P. and Chaves, M.P. (2014) Muscoid Diptera as potential vectors of bacterial agents on dairy farms in the northern region of Paraná, Brazil. Semin Ciênc Agrár 35, 3127-3138.
Almeida, L.M. and Mise, K.M. (2009) Diagnosis and key of the main families and species of south American Coleoptera of forensic importance. Revist Brasil de Ento 53, 227-244.
Almuzara, M., Barberis, C., Veiga, F., Bakai, R., Cittadini, R., Vera, R., Ocampo, C., Serena, M. et al. (2017) New unusual presentations of Comamonas kerstersii infection. Microb New Infect 19, 91-95.
Alves, T.S., Lara, G.H.B., Maluna, R.P., Ribeiro, M.G. and Leite, D.S. (2018) Carrier flies of multidrug-resistand Escherichia coli as potential dissemination agente in dairy farm environment. Sci Total Environ 633, 1354-1351.
Arsenopoulos, K.V., Triantafillou, E., Filioussis, G. and Papadopoulos, E. (2018) Fly repellency using deltamethrin may reduce intramammary infections of dairy cows under intensive management. Comp Immunol Microbiol infect Dis 61, 16-23.
Barreiro, J.R., Ferreira, C.R., Sanvido, G.B., Kostrzewa, M., Maier, T., Wegemann, B., Böttcher, V., Eberlin, M.N. et al. (2010) Short communication: Identification of subclinical cow mastitis pathogens in milk by matrix-assisted laser desorption/ionization time-of-flight mass spectrometry. J Dairy Sci 93, 5661-5667.
Bouamamaa, L., Sorlozano, A., Laglaoui, A., Lebbadi, M., Aarab, A. and Gutierrez, J. (2010) Antibiotic resistance patterns of bacterial strains isolated from Periplaneta americana and Musca domestica in Tangier, Morocco. JIDC 4, 194-201.
Braga, P.A.C., Gonçalves, J.L., Barreiro, J.R., Ferreira, C.R., Tomazi, T., Eberlin, M.N. and Santos, M.V. (2018) Rapid identification of bovine mastitis pathogens by MALDI-TOF mass spectrometry. Pesq Vet Bras 38, 586-594.
Carramaschi, I.N., Lopes, J.C.O., Leite, A.J., Carneiro, M.T., Barbosa, R.R., Boas, M.H.V., Rangel, K., Chagas, T.P.G. et al. (2021) Surveillance of antimicrobial resistant bacteria in flies (Diptera) in Rio de Janeiro city. Acta Trop 220, 105962.
Carvalho, C.J.B., Moura, M.O. and Ribeiro, P.B. (2002) Chave para adultos de dípteros (Muscidae, Fanniidae, Anthomyiidae) associados ao ambiente humano no Brasil. J Brasil Entomol 46, 107-144.
Carvalho, C.J.B. and Ribeiro, P.B. (2000) Chave de identificação das espécies de Calliphoridae (Diptera) do Sul do Brasil. Rev Bras Parasitol Vet 9, 169-173.
Castro, B.G., Souza, M.M.S. and Bittencourt, A.J. (2008) Isolamento de espécies enterobacterianas em Stomoxys calcitrans. Ciência Rural 38, 1-2657.
Castro, B.G., Souza, M.M.S., Regua, A.H., Regua, M.A.H. and Bittencourt, A.J. (2013) Occurence of Shiga toxigenic Escherichia coli in Stomoxys calcitrans (Diptera: Muscidae). J Bras de Parasitol Vet 22, 318-321.
Castro, B.G., Souza, M.M.S., Regua, M.A.H. and Bittencourt, A.J. (2016) Genetic relationship between Escherichia coli strains isolated from dairy mastitis and from the stable fly Stomoxys calcitrans. Pesq Vet Bras 36, 479-484.
Cheng, J., Zhou, M., Nobrega, D.B., Barkema, H.W., Xu, S., Li, M., Kastelic, J.P., Shi, Y. et al. (2020) Genetic diversity and molecular epidemiology of outbreaks of Klebsiella pneumoniae mastitis on two large Chinese dairy farms. J Dairy Sci 104, 762-775.
Cobirka, M., Tancin, V. and Slama, P. (2020) Review epidemiology and classification of mastitis animals. Animals 10, 2212.
Courtney, G.W., Pape, T., Skevington, J.H. and Sinclair, B.J. (2017) Biodiversity of Diptera. In Insect Biodiversity: Science and Society ed. Foottit, R.G. and Adler, P.H., 2nd edn. pp. 229-278. USA, Wiley-Blackwell.
Dean, A.G., Sullivan, K.M, and Soe M.M. (2019) Openepi: Open Source Epidemiologic Statistics for Public Health, Versão. https://www.openepi.com/SampleSize/SSPropor.htm, updated 2013/04/06, accessed 2019/02/25.
Dufour, S., Dohoo, I.R., Barkema, H.W., Descôteaux, L., Devries, T.J., Reyher, K.K., Roy, J.P. and Scholl, D.T. (2012) Epidemiology of coagulase negative staphylococci intramammary infection in dairy cattle and the effect of bacteriological culture misclassification. J Dairy Sci 95, 3110-3124.
Förster, M., Sievert, K., Messler, S., Klimpel, S. and Pfeffer, K. (2009) Comprehensive study on the occurrence and distribution of pathogenic microorganisms carried by synanthropic flies caught at different rural locations in Germany. J Med Entomol 46, 1164-1666.
Gao, X., Fan, C., Zhang, Z., Li, S., Xu, C., Zhao, Y., Han, L., Zhang, D. et al. (2020) Enterococcal isolates from bovine subclinical and clinical mastitis: antimicrobial resistance and integron-gene cassette distribution. Microb Pathog 129, 82-87.
Ghalehnoo, M.R. (2015) Housefly (Musca domestica) as carrier of enterotoxigenic Staphylococcus aureus in broiler farms in Iran: is it important for public health. Int J Enteric Pathog 3, 25688.
Gonçalves, J.L., Tomazi, T., Barreiro, J.R., Braga, P.A.C., Ferreira, C.R., Junior, J.P.A., Eberlin, M.N. and Santos, M.V. (2014) Identification of Corynebacterium spp. isolated from bovine intramammary infections by matrix-assisted laser desorption ionization-time of flight mass spectrometry. Vet Microbiol 173, 147-151.
Granja, B.M., Fidelis, C.E., Garcia, B.L.N. and Santos, M.V. (2021) Evaluation of chromogenic culture media for rapid identification of microorganisms isolated from cows with clinical and subclinical mastitis. J Dairy Sci 103, 9115-9129.
Guégan, M., Zauache, K., Démichel, C., Minard, G., Van, V.T., Potier, P., Mavingu, P. and Moro, C.V. (2018) The mosquito holobiont: fresh insight intomosquito-microbiota interactions. Microbiome 6, 49.
Guerra, S.T., Orsi, H., Joaquim, S.F., Guimarães, F.F., Lopes, B.C., Dalanezi, F.M., Leite, D.S., Langoni, H. et al. (2020) Short communication: Investigation of extra-intestinal pathogenic Escherichia coli virulence genes, bacterial motility, and multidrug resistance pattern of strains isolated from dairy cows with different severity scores of clinical mastitis. J Dairy Sci 103, 3606-3614.
Guimarães, F. F., Joaquim, S.F., Guerra, S. T., Dalanezi, F.M., Lopes, B. C., Pantoja, J.C.F., Ribeiro, M.G., Hernandes, R.T. et al. (2019). Etiology of clinical mastitis in high-yeld farms southeastern, Brazil. In: National Mastitis Council 58th Annual Meeting, 2019, Savannah. Vol. 1, pp. 186-187. Savannah, Georgia, EUA: Annual Meeting Proceeding.
Guimarães, F.F., Moraes, G.N., Joaquim, S.F., Guerra, S.T., Dalanezi, F.M., Lopes, B.C., Pantoja, J.C.F., Ribeiro, M.G. et al. (2020) Identification of Enterococcus spp. isolated from milk samples of clinical mastitis. In National Mastitis Council- NMC, n°59, Orlando- Florida. Vol. 28-31. pp. 195-196. Orlando- Florida, EUA: Annual Meeting Proceeding.
Gutiérrez-Chávez, A.J., Martínez-Ortega, E.A., Valencia-Posadas, M., León-Galván, M.F., Fuente-Salcido, N.M., Bideshi, D.K. and Barboza-Corona, J.E. (2016) Potential use of Bacillus thuringiensis bacteriocins to control antibiotic-resistant bacteria associated with mastitis in dairy goats. Folia Microbiol 61, 11-19.
Hladík, M., Lipovy, B., Kaloudova, Y., Hanslianova, M. and Vitkova, I. (2021) Human infections by Wohlfahrtiimonas chitiniclastica: a mini-review and the first report of a burn wound infection after accidental Myiasis in central. Europ Microorg 9, 1934.
Ioannou, P. (2019) Escherichia hermannii infections in humans: a systematic review. Trop Med Infect Dis 4, 17.
Jahan, N.A., Godden, S.M., Royster, S., Schoenfuss, T.C., Gebhart, C., Timmerman, J. and Fink, R.C. (2021) Evaluation of the matrix-assisted laser desorption ionization time of flight mass spectrometry (MALDI-TOF MS) system in the detection of mastitis pathogens from bovine milk samples. J Microbiol Methods 182, 106-168.
Junqueira, A.C., Ratan, A., Acerbi, E., Drautz-Moses, A.I., Balakrishnan, N.V., Premkrishnan, P.I., Bodo, L., Rikky, W. et al. (2017) The microbiomes of blowflies and houseflies as bacterial transmission reservoirs. Sci Rep 7, 16324.
Kaper, J.B., Nataro, J.P. and Mobley, H.L.T. (2004) Pathogenic Escherichia coli. Nat Rev Microbiol 2, 123-140.
Klaas, I.C. and Zadoks, R.N. (2018) An update on environmental mastitis: challenging perceptions. Transb Emerg Dis 65, 166-185.
Klotz, P., Higgin, P.G., Schaubmar, A.R., Failing, K., Leidner, U., Seifert, H., Scheufen, S., Semmler, T. et al. (2019) Seasonal occurrence and Carbapenem susceptibility of bovine Acinetobacter baumannii in Germany. Front Microbiol 10, 272.
Marcondes, C.B., and Thyssen, P.J. (2017) Flies. In Arthropod Borne Diseases ed. Marcondes, C.B. pp. 475-502. Switzerland: Springer International Publishing.
Mbuk, E.U., Kwaga, J.K.P., Bale, J.O.O., Boro, L.A. and Umoh, J.U. (2016) Coliform organisms associated with milk of cows with mastitis and their sensitivity to commonly available antibiotics in Kaduna state, Nigeria. JVMAH 8, 228-236.
Nazni, W.A., Luke, H., Wan Rozita, W.M., Abdullah, A.G., Sa'diyah, I., Azahari, A.H., Zamree, I., Tan, S.B. et al. (2005) Determination of the flight range and dispersal of the house fly, Musca domestica (L.) using mark release recapture technique. Trop Biomed 22, 53-61.
Oliveira, E.B., Tomaim, M.R., Silva, S.P. and Toledo, R.C.C. (2017) Caracterização da intoxicação alimentar causada pelo Bacillus cereus: uma revisão. Hig Alimentar 31, 268-269.
Onwugamba, F.C., Fitzgerald, J.R., Rochon, K., Luca Guardabassi, L., Alabi, A., Kühne, S., Grobusch, M.P. and Schaumburg, F. (2018) The role of ‘filth flies’ in the spread of antimicrobial resistance. Travel Med Infect Dis 22, 8-17.
Porcellato, D., Skeie, S.B., Mellegård, H., Monshaugen, M., Goransson, S.A., Aanrud, B., Lindstedt, M.A. and Aspholm, M. (2021) Characterization of Bacillus cereus sensu lato isolates from milk for consumption; phylogenetic identity, potential for spoilage and disease. Food Microbiol 93, 103604.
Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B., Casari, A.S. and Constantino, R. (2012a) Chave Para Ordens - Adultos. In Insetos do Brasil. Diversidade e Taxonomia ed. Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B., Casari, S.A. and Constantino, R. pp. 191-197 and 701-745. Ribeirão Preto, Brazil: Editora Holos.
Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B., Casari, A.S. and Constantino, R. (2012b) Coleoptera. In Insetos do Brasil. Diversidade e taxonomia ed. Rafael, J.A., Melo, G.A.R., Carvalho, C.J.B., Casari, S.A. and Constantino, R. pp. 453-537. Ribeirão Preto, Brazil: Editora Holos.
Rafael, J.A., Pimentel, F.S.P. and Godoi, R.J.P. (2009) The enigmatic genus Ctenostylum Macquart with the description of a new species from the Brazilian Amazon Basin and a checklist of world Ctenostylidae species (Diptera). Zootaxa 20, 63-68.
Rahuma, N., Ghenghesh, K.S., Ben Aissa, R. and Elamaari, A. (2005) Carriage by the housefly (Musca domestica) of multiple-antibiotic-resistant bacteria that are potentially pathogenic to humans, in hospital and other urban environments in Misurata, Libya. Ann Trop Med Parasitol 99, 795-802.
Ribeiro, M.C., Morais, A.B.C., Alves, A.C., Bolaños, C.A.D., Paula, C.L., Portilho, F.V.R., Júnior, G.V., Lara, G.H.B. et al. (2022) Klebsiella-induced infections in domestic species: a case-series study in 697 animals (1997-2019). Braz J Microbiol 53, 455-464.
Rodrigues, M.X., Lima, S.F., Higgins, C.H., Canniatti-Brazaca, S.G. and Bicalho, J. (2016) The Lactococcus genus as a potential emerging mastitis pathogen group: a report on an outbreak investigation. Dairy Sci 99, 9864-9874.
Ruegg, P. (2017) Review: Mastitis detection, management, and prevention. J Dairy Sci 100, 10381-10397.
Ryan, M.P. and Pembroke, J.T. (2020) The genus Ochrobactrum as major opportunistic. Pathog Microorg 8, 1797.
Sadashiv, S.O. and Kaliwal, B.B. (2014) Isolation, characterization and antibiotic resistance of Bacillus sps. from bovine mastitis in the region of North Karnataka, India. Int J Curr Microbiol Appl Sci 3, 360-373.
Sarwar, M. (2015) Insect vectors involving in mechanical transmission of human pathogens for serious diseases international. J Bioinf Biomed Eng 3, 300-306.
Scaccabarozzi, C., Locatelli, G., Pisoni, G., Manarolla, A., Casula, V. and Moroni, P. (2011) Short communication: Epidemiology and genotyping of Candida rugosa strains responsible for persistent intramammary infections in dairy cows. J Dairy Sci 94, 4574-4577.
Schukken, Y., Chuff, M., Moroni, P., Gurjar, A., Santisteban, C., Belomestnykh, N. and Zadocks, R.N. (2012) Randomized clinical trial to evaluate the efficacy of 5-day ceftiofur hydrochloride intramammary treatment on nonsevere gram-negative clinical mastitis. J Dairy Sci 94, 6203-6215.
Song, X., Huangc, X., Xuc, H., Zhang, C., Chena, S., Liua, F., Guana, S., Zhanga, S. et al. (2020) The prevalence of pathogens causing bovine mastitis and their associated risk factors in 15 large dairy farms in China: an observational study. Vet Microbiol 247, 108757.
Storms, V., Devriese, L.A., Coopman, R., Schumann, P., Vyncke, F. and Gillis, M. (2003) Arthrobacter gandavensis sp. nov., for strains of veterinary origin. Int J Syst Evol Microbiol 53, 1881-1188.
Yoon, S. and Lee, Y.J. (2021) Molecular characteristics of Enterococcus faecalis and Enterococcus faecium from Bulk tank milk in Korea. Animals 11, 661.

Auteurs

A B Bertolini (AB)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

A M Prado (AM)

Department of Animal Biology, Biology Institute, University of Campinas-UNICAMP, Campinas, SP, Brazil.

P J Thyssen (PJ)

Department of Animal Biology, Biology Institute, University of Campinas-UNICAMP, Campinas, SP, Brazil.

M de Souza Ribeiro Mioni (M)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

F L R de Gouvea (FLR)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

D da Silva Leite (D)

Department of Genetics, Evolution, Microbiology and Immunology, UNICAMP, Campinas, SP, Brazil.

H Langoni (H)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

J C de Figueiredo Pantoja (JC)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

V M Rall (VM)

Department of Microbiology and Immunology, UNESP, Botucatu, SP, Brazil.

F F Guimarães (FF)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

S F Joaquim (SF)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

S T Guerra (ST)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

R T Hernandes (RT)

Department of Microbiology and Immunology, UNESP, Botucatu, SP, Brazil.

S B Lucheis (SB)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

M G Ribeiro (MG)

Department of Animal Production and Preventive Veterinary Medicine, School of Veterinary Medicine and Animal Sciences, São Paulo State University-UNESP, Botucatu, SP, Brazil.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH