Volume 7, Issue 2 (June 2020)
J. Food Qual. Hazards Control 2020, 7(2): 67-74 |
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Machado M, Ribeiro W, Toledo V, Ramos G, Vigoder H, Nascimento J. Antibiotic Resistance and Biofilm Production in Catalase-Positive Gram-Positive Cocci Isolated from Brazilian Pasteurized Milk. J. Food Qual. Hazards Control 2020; 7 (2) :67-74
URL: http://jfqhc.ssu.ac.ir/article-1-676-en.html
URL: http://jfqhc.ssu.ac.ir/article-1-676-en.html
Laboratório de Microbiologia, Instituto Federal de Educação, Ciência e Tecnologia do Rio de Janeiro (IFRJ), Rio de Janeiro, RJ, Brazil , janaina.nascimento@ifrj.edu.br
Abstract: (2178 Views)
Background: Milk is a reservoir for several groups of microorganisms, which may pose health risks. The aim of this work was to assess the antibiotic resistance and biofilm production in catalase-positive Gram-positive cocci isolated from Brazilian pasteurized milk.
Methods: The bacteria were isolated using Baird-Parker agar and identified by Matrix-Assisted Laser Desorption/Ionization-Time-Of-Flight (MALDI-TOF) mass spectrometer. Disk diffusion technique was used to evaluate antimicrobial susceptibility. For qualitative evaluation of biofilm production, the growth technique was used on Congo Red Agar.
Results: Totally, 33 out of 64 isolates were identified, including Staphylococcus epidermidis (n=3; 4.7%), Macrococcus caseolyticus (n=14; 21.9%), and Kocuria varians (n=16; 25%). Twenty-two isolates were resistant to at least one antibiotic. Biofilm production was detected in only 5 isolates of K. varians and 1 isolate of S. epidermidis. All 14 M. caseolyticus isolates were resistant to at least one antibiotic; but, multidrug resistant (MDR) isolates were not detected. Among all K. varians isolates, 4 were resistant to at least one antibiotic from three different classes and were considered to be MDR.
Conclusion: The presence of antibiotic-resistant M. caseolyticus, S. epidermidis, and K. varians isolates, especially MDRs, in milk samples highlights the possible role of milk as a reservoir of resistance genes.
DOI: 10.18502/jfqhc.7.2.2886
Methods: The bacteria were isolated using Baird-Parker agar and identified by Matrix-Assisted Laser Desorption/Ionization-Time-Of-Flight (MALDI-TOF) mass spectrometer. Disk diffusion technique was used to evaluate antimicrobial susceptibility. For qualitative evaluation of biofilm production, the growth technique was used on Congo Red Agar.
Results: Totally, 33 out of 64 isolates were identified, including Staphylococcus epidermidis (n=3; 4.7%), Macrococcus caseolyticus (n=14; 21.9%), and Kocuria varians (n=16; 25%). Twenty-two isolates were resistant to at least one antibiotic. Biofilm production was detected in only 5 isolates of K. varians and 1 isolate of S. epidermidis. All 14 M. caseolyticus isolates were resistant to at least one antibiotic; but, multidrug resistant (MDR) isolates were not detected. Among all K. varians isolates, 4 were resistant to at least one antibiotic from three different classes and were considered to be MDR.
Conclusion: The presence of antibiotic-resistant M. caseolyticus, S. epidermidis, and K. varians isolates, especially MDRs, in milk samples highlights the possible role of milk as a reservoir of resistance genes.
DOI: 10.18502/jfqhc.7.2.2886
Type of Study: Original article |
Subject:
Special
Received: 20/04/16 | Accepted: 20/05/22 | Published: 20/06/18
Received: 20/04/16 | Accepted: 20/05/22 | Published: 20/06/18
References
1. Alegbeleye O.O., Guimarães J.T., Cruz A.G., Sant'Ana A.S. (2018). Hazards of a 'healthy'trend? An appraisal of the risks of raw milk consumption and the potential of novel treatment technologies to serve as alternatives to pasteurization. Trends in Food Science and Technology. 82: 148-166. [DOI: 10.1016/j.tifs.2018.10.007] [DOI:10.1016/j.tifs.2018.10.007]
2. Ali N.M., Sarwar K., Mazhar S.A., Liaqat I., Andleeb S., Mazhar B., Kalim B. (2017). Effect of medicinal plants, heavy metals and antibiotics against pathogenic bacteria isolated from raw, boiled and pasteurized milk. Pakistan Journal of Pharmaceutical Sciences. 30: 2173-2182.
3. Benkerroum N. (2018). Staphylococcal enterotoxins and enterotoxin-like toxins with special reference to dairy products: an overview. Critical Reviews in Food Science and Nutrition. 58: 1943-1970. [DOI: 10.1080/10408398.2017.1289149] [DOI:10.1080/10408398.2017.1289149] [PMID]
4. Carpentier B., Chassaing D. (2004). Interactions in biofilms between Listeria monocytogenes and resident microorganisms from food industry premises. International Journal of Food Microbiology. 97: 111-122. [DOI: 10.1016/j.ijfoodmicro.2004. 03.031] [DOI:10.1016/j.ijfoodmicro.2004.03.031] [PMID]
5. Castro R.D., Pedroso S.H.S.P., Sandes S.H.C., Silva G.O., Luiz K.C.M., Dias R.S., Filho R.A.T., Figueiredo H.C.P., Santos S.G., Nunes A.C., Souza M.R. (2020). Virulence factors and antimicrobial resistance of Staphylococcus aureus isolated from the production process of Minas artisanal cheese from the region of Campo das Vertentes, Brazil. Journal of Dairy Science. 103: 2098-2110. [DOI: 10.3168/jds.2019-17138] [DOI:10.3168/jds.2019-17138] [PMID]
6. Chajęcka-Wierzchowska W., Zadernowska A., Gajewska J. (2019). S. epidermidis strains from artisanal cheese made from unpasteurized milk in Poland-Genetic characterization of antimicrobial resistance and virulence determinants. International Journal of Food Microbiology. 294: 55-59. [DOI: 10.1016/j.ijfoodmicro.2019.02.004] [DOI:10.1016/j.ijfoodmicro.2019.02.004] [PMID]
7. Clinical and Laboratory Standards Institute (CLSI). (2018). Performance standards for antimicrobial susceptibility testing. 28th edition. CLSI supplement M100. Wayne, PA.
8. Cruzado-Bravo M.L.M., Silva N.C.C., Rodrigues M.X., Silva G.O.E., Porto E., Sturion G.L. (2019). Phenotypic and genotypic characterization of Staphylococcus spp. isolated from mastitis milk and cheese processing: study of adherence and biofilm formation. Food Research International. 122: 450-460. [DOI: 10.1016/j.foodres.2019.04.017]. [DOI:10.1016/j.foodres.2019.04.017] [PMID]
9. Donlan R.M. (2002). Biofilms: microbial life on surfaces. Emerging Infectious Diseases. 8: 881-890. [DOI: 10.3201/eid0809. 020063] [DOI:10.3201/eid0809.020063] [PMID] [PMCID]
10. El-Ashker M., Gwida M., Tomaso H., Monecke S., Ehricht R., El-Gohary F., Hotzel H. (2015). Staphylococci in cattle and buffaloes with mastitis in Dakahlia Governorate, Egypt. Journal of Dairy Science. 98: 7450-7459. [DOI: 10.3168/jds. 2015-9432] [DOI:10.3168/jds]
11. Eladli M.G., Alharbi N.S., Khaled J.M., Kadaikunnan S., Alobaidi A.S., Alyahya S.A. (2019). Antibiotic-resistant Staphylococcus epidermidis isolated from patients and healthy students comparing with antibiotic-resistant bacteria isolated from pasteurized milk. Saudi Journal of Biological Sciences. 26: 1285-1290. [DOI: 10.1016/j.sjbs.2018.05.008] [DOI:10.1016/j.sjbs.2018.05.008] [PMID] [PMCID]
12. Fabres-Klein M.H., Santos M.J.C., Klein R.C., de Souza G.N., Ribon A.D.O.B. (2015). An association between milk and slime increases biofilm production by bovine Staphylococcus aureus. BioMed Central Veterinary Research. 11: 3. [DOI: 10.1186/s12917-015-0319-7] [DOI:10.1186/s12917-015-0319-7] [PMID] [PMCID]
13. Freeman D.J., Falkiner F.R., Keane C.T. (1989). New method for detecting slime production by coagulase negative staphylococci. Journal of Clinical Pathology. 42: 872-874. [DOI: 10.1136/ jcp.42.8.872] [DOI:10.1136/jcp.42.8.872]
14. Gutierrez D., Delgado S., Vazquez-Sanchez D., Martinez B., Cabo M.L., Rodriguez A., Herrera J.J., Garcia P. (2012). Incidence of Staphylococcus aureus and analysis of associated bacterial communities on food industry surfaces. Applied and Environmental Microbiology. 78: 8547-8554. [DOI: 10.1128/ AEM. 02045-12] [DOI:10.1128/AEM.02045-12]
15. International Organization for Standardization (ISO). (1999). Microbiology of food and animal feeding stuffs-Horizontal method for the enumeration of coagulase-positive staphylococci (Staphylococcus aureus and other species): part 1: technique using Baird-Parker agar medium. No. 6888-1.
16. Joishy T.K., Dehingia M., Khan M.R. (2019). Bacterial diversity and metabolite profiles of curd prepared by natural fermentation of raw milk and back sloping of boiled milk. World Journal of Microbiology and Biotechnology. 35: 102. [DOI: 10.1007/s11274-019-2677-y] [DOI:10.1007/s11274-019-2677-y] [PMID]
17. Kačániová M., Kunová S., Nagyová Ľ., Horská E., Haščík P., Terentjeva M. (2019). Application of MALDI-TOF mass spectrometry for identification of bacteria isolated from traditional Slovak cheese "parenica". Journal of Microbiology, Biotechnology and Food Sciences. 8: 1294-1297. [DOI: 10.15414/ jmbfs.2019.8.6.1294-1297] [DOI:10.15414/jmbfs.2019.8.6.1294-1297]
18. Kim S.J., Moon D.C., Park S.C., Kang H.Y., Na S.H., Lim S.K. (2019). Antimicrobial resistance and genetic characterization of coagulase-negative staphylococci from bovine mastitis milk samples in Korea. Journal of Dairy Science. 102: 11439-11448. [DOI: 10.3168/jds.2019-17028] [DOI:10.3168/jds.2019-17028] [PMID]
19. Kloos W.E., Ballard D.N., George C.G., Webster J.A., Hubner R.J., Ludwig W., Schleifer K.H., Fiedler F., Schubert K. (1998). Delimiting the genus Staphylococcus through description of Macrococcus caseolyticus gen. nov., comb. nov. and Macrococcus equipercicus sp. nov., and Macrococcus bovicus sp. nov. and Macrococcus carouselicus sp. nov. International Journal of Systematic and Evolutionary Microbiology. 48: 859-877. [DOI: 10.1099/00207713-48-3-859] [DOI:10.1099/00207713-48-3-859] [PMID]
20. Knight G.C., Nicol R.S., McMeekin T.A. (2004). Temperature step changes: a novel approach to control biofilms of Streptococcus thermophilus in a pilot plant-scale cheese-milk pasteurization plant. International Journal of Food Microbiology. 93: 305-318. [DOI: 10.1016/j.ijfoodmicro.2003.11.013] [DOI:10.1016/j.ijfoodmicro.2003.11.013] [PMID]
21. Leriche V., Briandet R., Carpentier B. (2003). Ecology of mixed biofilms subjected daily to a chlorinated alkaline solution: spatial distribution of bacterial species suggests a protective effect of one species to another. Environmental Microbiology. 5: 64-71. [DOI: 10.1046/j.1462-2920.2003.00394.x] [DOI:10.1046/j.1462-2920.2003.00394.x] [PMID]
22. MacFadyen A.C., Fisher E.A., Costa B., Cullen C., Paterson G.K. (2018). Genome analysis of methicillin resistance in Macrococcus caseolyticus from dairy cattle in England and Wales. Microbial Genomics. 4: 1-8. [DOI: 10.1099/mgen.0. 000191] [DOI:10.1099/mgen.0.000191] [PMID] [PMCID]
23. Martinez B.A., Stratton J., Bianchini A. (2017). Isolation and genetic identification of spore-forming bacteria associated with concentrated-milk processing in Nebraska. Journal of Dairy Science. 100: 919-932. [DOI: 10.3168/jds.2016-11660] [DOI:10.3168/jds.2016-11660] [PMID]
24. Mnif S., Jardak M., Yaich A., Aifa S. (2020). Enzyme-based strategy to eradicate monospecies Macrococcus caseolyticus biofilm contamination in dairy industries. International Dairy Journal. 100: 104560. [DOI: 10.1016/j.idairyj.2019.104560] [DOI:10.1016/j.idairyj.2019.104560]
25. Mogha K.V., Shah N.P., Prajapati J.B., Chaudhari A.R. (2014). Biofilm - a threat to dairy industry. Indian Journal of Dairy Science. 67: 459-466. [DOI: 10.1111/1471-0307.12171] [DOI:10.1111/1471-0307.12171]
26. Møretrø M., Langsrud S. (2017). Residential bacteria on surfaces in the food industry and their implications for food safety and quality. Comprehensive Reviews in Food Science and Food Safety. 16: 1022-1041. [DOI: 10.1111/1541-4337.12283] [DOI:10.1111/1541-4337.12283]
27. Nawaz M., Wang J., Zhou A., Ma C., Wu X., Moore J.E., Millar B.C., Xu J. (2011). Characterization and transfer of antibiotic resistance in lactic acid bacteria from fermented food products. Current Microbiology. 62: 1081-1089. [DOI: 10.1007/s00284-010-9856-2] [DOI:10.1007/s00284-010-9856-2] [PMID]
28. Organji S.R., Abulreesh H.H., Elbanna K., Osman G.H.E., Almalki M.H.K. (2018). Diversity and characterization of Staphylococcus spp. in food and dairy products: a foodstuff safety assessment. Journal of Microbiology, Biotechnology and Food Sciences. 7: 586-593. [DOI: 10.15414/jmbfs.2018.7.6.586-593] [DOI:10.15414/jmbfs.2018.7.6.586-593]
29. Osman K.M., Pires A.D.S., Franco O.L., Orabi A., Hanafy M.H., Marzouk E., Hussein H., Alzaben F.A., Almuzaini A.M., Elbehiry A. (2019). Enterotoxigenicity and antibiotic resistance of coagulase-negative staphylococci isolated from raw buffalo and cow milk. Microbial Drug Resistance. 26: 520-530. [DOI: 10.1089/mdr.2019.0114] [DOI:10.1089/mdr.2019.0114] [PMID]
30. Purty S., Saranathan R., Prashanth K., Narayanan K., Asir J., Devi C.S., Kumar Amarnath S. (2013). The expanding spectrum of human infections caused by Kocuria species: a case report and literature review. Emerging Microbes and Infections. 2: 1-8. [DOI: 10.1038/emi.2013.71] [DOI:10.1038/emi.2013.71] [PMID] [PMCID]
31. Ribeiro-Júnior J.C., Tamanini R., de Oliveira A.L.M., Alfieri A.A., Beloti V. (2018). Genetic diversity of thermoduric spoilage microorganisms of milk from Brazilian dairy farms. Journal of Dairy Science. 101: 6927-6936. [DOI: 10.3168/jds.2017-13948] [DOI:10.3168/jds.2017-13948] [PMID]
32. Røder H.L., Raghupathi P.K., Herschend J., Brejnrod A., Knøchel S., Sørensen S.J., Burmølle M. (2015). Interspecies interactions result in enhanced biofilm formation by co-cultures of bacteria isolated from a food processing environment. Food Microbiology. 51: 18-24. [DOI: 10.1016/j.fm.2015.04.008] [DOI:10.1016/j.fm.2015.04.008] [PMID]
33. Rodriguez-Alonso P., Fernandez-Otero C., Centeno J.A., Garabal J.I. (2009). Antibiotic resistance in lactic acid bacteria and Micrococcaceae/Staphylococcaceae isolates from artisanal raw milk cheeses, and potential implications on cheese making. Journal of Food Science. 74: M284-M293. [DOI: 10.1111/j.1750-3841.2009.01217.x.] [DOI:10.1111/j.1750-3841.2009.01217.x] [PMID]
34. Ruegg P.L. (2017). A 100-year review: mastitis detection, management, and prevention. Journal of Dairy Science. 100: 10381-10397. [DOI: 10.3168/jds.2017-13023] [DOI:10.3168/jds.2017-13023] [PMID]
35. Sanchez-Vizuete P., Orgaz B., Aymerich S., Le Coq D., Briandet R. (2015). Pathogens protection against the action of disinfectants in multispecies biofilms. Frontiers in Microbiology. 6: 705. [DOI: 10.3389/fmicb.2015.00705] [DOI:10.3389/fmicb.2015.00705] [PMID] [PMCID]
36. Schwendener S., Cotting K., Perreten V. (2017). Novel methicillin resistance gene mecD in clinical Macrococcus caseolyticus strains from bovine and canine sources. Scientific Reports. 7: 43797. [DOI: 10.1038/srep43797] [DOI:10.1038/srep43797] [PMID] [PMCID]
37. Song M., Li Q., Zhang Y., Song J., Shi X., Shi C. (2016). Biofilm formation and antibiotic resistance pattern of dominant Staphylococcus aureus clonal lineages in China. Journal of Food Safety. 37: e12304. [DOI: 10.1111/jfs.12304] [DOI:10.1111/jfs.12304]
38. Stackebrandt E., Koch C., Gvozdiak O., Schumann P. (1995). Taxonomic dissection of the genus Micrococcus: Kocuria gen. nov., Nesterenkonia gen. nov., Kytococcus gen. nov., Dermacoccus gen. nov., and Micrococcus Cohn 1872 gen. emend. International Journal of Systematic and Evolutionary Microbiology. 45: 682-692. [DOI: 10.1099/00207713-45-4-682] [DOI:10.1099/00207713-45-4-682] [PMID]
39. Thomas C.M., Nielsen K.M. (2005). Mechanisms of, and barriers to, horizontal gene transfer between bacteria. Nature Reviews Microbiology. 3: 711-721. [DOI: 10.1038/nrmicro1234] [DOI:10.1038/nrmicro1234] [PMID]
40. Tóth A.G., Csabai I., Krikó E., Tozser D., Maróti G., Patai Á.V., Makrai L., Szita G., Solymosi N. (2019). Raw milk for human consumption may carry antimicrobial resistance genes. BioRxiv. [DOI: 10.1101/853333] [DOI:10.1101/853333]
41. Vanderhaeghen W., Cerpentier T., Adriaensen C., Vicca J., Hermans K., Butaye P. (2010). Methicillin-resistant Staphylococcus aureus (MRSA) ST398 associated with clinical and subclinical mastitis in Belgian cows. Veterinary Microbiology. 144: 166-171. [DOI: 10.1016/j.vetmic.2009. 12.044] [DOI:10.1016/j.vetmic.2009.12.044] [PMID]
42. Vignaroli C., Zandri G., Aquilanti L., Pasquaroli S., Biavasco F. (2011). Multidrug-resistant enterococci in animal meat and faeces and co-transfer of resistance from an Enterococcus durans to a human Enterococcus faecium. Current Microbiology. 62: 1438-1447. [DOI: 10.1007/s00284-011-9880-x] [DOI:10.1007/s00284-011-9880-x] [PMID]
43. Yuan L., Burmølle M., Sadiq F.A., Wang N., He G. (2018). Interspecies variation in biofilm-forming capacity of psy-chrotrophic bacterial isolates from Chinese raw milk. Food Control. 91: 47-57. [DOI: 10.1016/j.foodcont.2018.03.026] [DOI:10.1016/j.foodcont.2018.03.026]
44. Yuan L., Hansen M.F., Røder H.L., Wang N., Burmølle M., He G. (2019). Mixed-species biofilms in the food industry: current knowledge and novel control strategies. Critical Reviews in Food Science and Nutrition. 1: 1-17. [DOI:10.1080/10408398. 2019.1632790] [DOI:10.1080/10408398.2019.1632790] [PMID]
45. Zhang W., Yu D., Sun Z., Chen X., Bao Q., Meng H., Hu S., Zhang H. (2008). Complete nucleotide sequence of plasmid plca36 isolated from Lactobacillus casei Zhang. Plasmid. 60: 131-135. [DOI: 10.1016/j.plasmid.2008.06.003] [DOI:10.1016/j.plasmid.2008.06.003] [PMID]
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