Abstract
The present study aims to quantify biofilm formation and determine the drug resistance profile of Staphylococcus aureus isolated from raw, pasteurized and ultra-high temperature (UHT) milk. Detection of S. aureus was made in 90 cow milk samples (30 raw, 30 pasteurized and 30 UHT). Biofilm biomass quantification was performed in 96-well polystyrene plates using the crystal violet technique. The resistance profile was determined by the disc-diffusion test. S. aureus was detected in 24.4% (22/90) of milk samples, with the highest prevalence in pasteurized milk. Biofilm production was observed in 100% of the S. aureus isolates from pasteurized and UHT milk, and in 81.8% of the strains from raw milk. Biofilm production by S. aureus drug-resistant strains was detected in 46.7% (14/30) of the isolates. In order to mitigate this problem, it is recommended to apply appropriate hygiene practices along the milk production chain.
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Agarwal A, Awasthi V, Dua A, Ganguly S, Garg V, Marwaha SS (2012) Microbiological profile of milk: impact of household practices. Indian J Public Health 56:88–94
Almatroudi A, Tahir S, Hu H, Chowdhury D, Gosbell IB, Jensen SO, Whiteley GS, Deva AK, Glasbey T, Vickery K (2017) Staphylococcus aureus dry surface biofilms are more resistant to heat treatment than traditional hydrated biofilms. J Hosp Infect 98:161–167
Arcuri EF, Ângelo FF, Guimarães MFM, Talon R, Borges MF, Leroy S, Loiseau G, Lange CC, Andrade NJ, Montet D (2010) Toxigenic status of Staphylococcus aureus isolated from bovine raw milk and minas frescal cheese in Brazil. J Food Prot 73:2225–2231
Ayele Y, Gutema FD, Edao BM, Girma R, Tufa TB, Beyene TJ, Tadesse F, Geloye M, Beyi AF (2017) Assessment of Staphylococcus aureus along milk value chain and its public health importance in Sebeta, central Oromia, Ethiopia. BMC Microbiol 17:141
Basanisi MG, La Bella G, Nobili G, Franconieri I, La Salandra G (2017) Genotyping of methicillin-resistant Staphylococcus aureus (MRSA) isolated from milk and dairy products in South Italy. Food Microbiol 62:141–146
Ceniti C, Britti D, Santoro AML, Musarella R, Ciambrone L, Casalinuovo F, Costanzo N (2017) Phenotypic antimicrobial resistance profile of isolates causing clinical mastitis in dairy animals. Ital J Food Saf 6:6612
Chudobova D, Dostalova S, Blazkova I, Michalek P, Ruttkay-Nedecky B, Sklenar M, Nejdl L, Kudr J, Gumulec J, Tmejova K, Konecna M, Vaculovicova M, Hynek D, Masarik M, Kynicky J, Kizek R, Adam V (2014) Effect of ampicillin, streptomycin, penicillin and tetracycline on metal resistant and non-resistant Staphylococcus aureus. Int J Environ Res Public Health 11:3233–3255
CLSI Clinical and Laboratory Standards Institute (2012) Performance standards for antimicrobial susceptibility testing; twenty-fifth informational supplement M100-S25 25-3
Costa FN, Belo NO, Costa EA, Andrade GI, Pereira LS, Carvalho IA, Santos RL (2018) Frequency of enterotoxins, toxic shock syndrome toxin-1, and biofilm formation genes in Staphylococcus aureus isolates from cows with mastitis in the Northeast of Brazil. Trop Anim Health Prod 50:1089–1097
Fabres-Klein MH, Santos MJC, Klein RC, Souza GN, Ribon AOB (2015) An association between milk and slime increases biofilm production by bovine Staphylococcus aureus. BMC Vet Res 11:3
Fejzic N, Begagic M, Šerić-Haračić S, Smajlovic M (2014) Beta lactam antibiotics residues in cow’s milk: comparison of efficacy of three screening tests used in Bosnia and Herzegovina. Bosn J Basic Med Sci 14:155–159
Hassan A, Usman J, Kaleem F, Omair M, Khalid A, Iqbal M (2011) Evaluation of different detection methods of biofilm formation in the clinical isolates. Braz J Infect Dis 15:305–311
Kamaruzzaman NF, Chong SQY, Edmondson-Brown KM, Ntow-Boahene W, Bardiau M, Good L (2017) Bactericidal and anti-biofilm effects of polyhexamethylene biguanide in models of intracellular and biofilm of Staphylococcus aureus isolated from bovine mastitis. Front Microbiol 8:1518
Knappstein K, Aust V, Kunz HJ, Kaske M (2013) Efficiency of two commercial on-farm pasteurizers for inactivation of mastitis pathogens in milk intended for feeding of calves. Berl Munch Tierarztl Wochenschr 126:32–36
Lee SHI, Mangolin BLC, Gonçalves JL, Neeff DV, Silva MP, Cruz AG, Oliveira CAF (2014) Biofilm-producing ability of Staphylococcus aureus isolates from Brazilian dairy farms. J Dairy Sci 97:1812–1816
Lira MC, Givisiez PE, De Sousa FG, Magnani M, De Souza EL, Spricigo DA, Gebreyes WA, De Oliveira CJ (2016) Biofilm-forming and antimicrobial resistance traits of staphylococci isolated from goat dairy plants. J Infect Dev Ctries 10:932–938
Liu H, Li S, Meng L, Dong L, Zhao S, Lan X, Wang J, Zheng N (2017) Prevalence, antimicrobial susceptibility, and molecular characterization of Staphylococcus aureus isolated from dairy herds in northern China. J Dairy Sci 100(8796):8803
Martini CL, Lange CC, Brito MA, Ribeiro JB, Mendonça LC, Vaz EK (2017) Characterisation of penicillin and tetracycline resistance in Staphylococcus aureus isolated from bovine milk samples in Minas Gerais, Brazil. J Dairy Res 84:202–205
McMillan K, Moore SC, McAuley CM, Fegan N, Fox EM (2016) Characterization of Staphylococcus aureus isolates from raw milk sources in Victoria, Australia. BMC Microbiol 16:169
Ou Q, Zhou J, Lin D, Bai C, Zhang T, Lin J, Zheng H, Wang X, Ye J, Ye X, Yao Z (2017) A large meta-analysis of the global prevalence rates of S. aureus and MRSA contamination of milk. Crit Rev Food Sci Nutr 7:1–16
Owusu-Kwarteng J, Wuni A, Akabanda F, Tano-Debrah K, Jespersen L (2017) Prevalence, virulence factor genes and antibiotic resistance of Bacillus cereus sensu lato isolated from dairy farms and traditional dairy products. BMC Microbiol 17:65
Papadopoulos P, Papadopoulos T, Angelidis AS, Boukouvala E, Zdragas A, Papa A, Hadjichristodoulou C, Sergelidis D (2018) Prevalence of Staphylococcus aureus and of methicillin-resistant S. aureus (MRSA) along the production chain of dairy products in north-western Greece. Food Microbiol 69:43–50
Picoli T, Peter CM, Zani JL, Waller SB, Lopes MG, Boesche KN, Vargas GDÁ, Hübner SO, Fischer G (2017) Melittin and its potential in the destruction and inhibition of the biofilm formation by Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa isolated from bovine milk. Microb Pathog 112:57–62
Pinheiro L, Mello PL, Abraão LM, Corrente JE, Cunha MLRS (2018) Evaluation of reference values for phenotypic tests to detect oxacillin resistance in coagulase-negative staphylococci. Future Microbiol 13:565–575
Rall VL, Vieira VL, Vieira FP, Rall R, Vieitis RL, Fernandes A Jr, Candeias JM, Cardoso JM, Cardoso KF, Araújo JP Jr (2008) PCR detection of staphylococcal enterotoxin genes in Staphylococcus aureus strains isolated from raw and pasteurized milk. Vet Microbiol 132:408–413
Richter K, Van den Driessche F, Coenye T (2017) Innovative approaches to treat Staphylococcus aureus biofilm-related infections. Essays Biochem 61:61–70
Seixas R, Varanda D, Bexiga R, Tavares L, Oliveira M (2015) Biofilm-formation by Staphylococcus aureus and Staphylococcus epidermidis isolates from subclinical mastitis in conditions mimicking the udder environment. Pol J Vet Sci 18:787–792
Sergelidis D, Angelidis AS (2017) Methicillin-resistant Staphylococcus aureus: a controversial food-borne pathogen. Lett Appl Microbiol 64:409–418
Sharma V, Sharma S, Dahiya DK, Khan A, Mathur M, Sharma A (2017) Coagulase gene polymorphism, enterotoxigenecity, biofilm production, and antibiotic resistance in Staphylococcus aureus isolated from bovine raw milk in North West India. Ann Clin Microbiol Antimicrob 16:65
Singh AK, Prakash P, Achra A, Singh GP, Das A, Singh RK (2017) Standardization and classification of in vitro biofilm formation by clinical isolates of Staphylococcus aureus. J Glob Infect Dis 9:93–101
Srednik ME, Tremblay YDN, Labrie J, Archambault M, Jacques M, Fernández Cirelli M, Gentilini ER (2017) Biofilm formation and antimicrobial resistance genes of coagulase-negative staphylococci isolated from cows with mastitis in Argentina. FEMS Microbiol Lett 364:fnx001
Tremblay YD, Lamarche D, Chever P, Haine D, Messier S, Jacques M (2013) Characterization of the ability of coagulase-negative staphylococci isolated from the milk of Canadian farms to form biofilms. J Dairy Sci 96:234–246
Vahedi M, Nasrolahei M, Sharif M, Mirabi AM (2013) Bacteriological study of raw and unexpired pasteurized cow’s milk collected at the dairy farms and super markets in Sari city in 2011. J Prev Med Hyg 54:120–123
Vergara A, Normanno G, Di Ciccio P, Pedonese F, Nuvoloni R, Parisi A, Santagada G, Colagiorgi A, Zanardi E, Ghidini S, Ianieri A (2017) Biofilm formation and its relationship with the molecular characteristics of food-related methicillin-resistant Staphylococcus aureus (MRSA). J Food Sci 82:2364–2370
Vittori J, Schocken-Iturrino RP, Poiatti ML, Pigatto CP, Chioda TP, Ribeiro CAM, Garcia GR, Ragazani AVF (2008) Microbiological quality of UHT goat milk: research of bacteria Staphylococcus, Bacillus and Clostridium genus. Ciência Rural 38:761–765
Yahav D, Paul M, Fraser A, Sarid N, Leibovici L (2007) Efficacy and safety of cefepime: a systematic review and meta-analysis. Lancet Infec Dis 7:338–348
Zeinhom MM, Abdel-Latef GK, Jordan K (2015) The use of multiplex PCR to determine the prevalence of enterotoxigenic Staphylococcus aureus isolated from raw milk, feta cheese, and hand swabs. J Food Sci 80:M2932–M2936
Zhang L, Li Y, Bao H, Wei R, Zhou Y, Zhang H, Wang R (2016) Population structure and antimicrobial profile of Staphylococcus aureus strains associated with bovine mastitis in China. Microb Pathog 97:103–109
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Costa, R.A., de Lira, J.V. & Aragão, M.F. Biofilm-formation by drug-resistant Staphylococcus aureus from cow milk. J Consum Prot Food Saf 14, 63–69 (2019). https://doi.org/10.1007/s00003-018-1186-5
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DOI: https://doi.org/10.1007/s00003-018-1186-5