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http://dx.doi.org/10.5851/kosfa.2022.e1

Isolation and Characterization of Halophilic Kocuria salsicia Strains from Cheese Brine  

Youn, Hye-Young (Center for One Health, College of Veterinary Medicine, Department of Veterinary Public Health, Konkuk University)
Seo, Kun-Ho (Center for One Health, College of Veterinary Medicine, Department of Veterinary Public Health, Konkuk University)
Publication Information
Food Science of Animal Resources / v.42, no.2, 2022 , pp. 252-265 More about this Journal
Abstract
Kocuria salsicia can survive in extreme environments and cause infections, including catheter-related bacteremia, in humans. Here, we investigated and evaluated the characteristics of nine K. salsicia strains (KS1-KS9) isolated from cheese brine from a farmstead cheese-manufacturing plant in Korea from June to December, 2020. Staphylococcus aureus American Type Culture Collection (ATCC) 29213 was used as a positive control in the growth curve analysis and biofilm-formation assays. All K. salsicia isolates showed growth at 15% salt concentration and temperatures of 15℃, 25℃, 30℃, 37℃, and 42℃. KS6 and KS8 showed growth at 5℃, suggesting that they are potential psychrotrophs. In the biofilm-formation analysis via crystal violet staining, KS6 exhibited the highest biofilm-forming ability at various temperatures and media [phosphate buffered saline, nutrient broth (NB), and NB containing 15% sodium chloride]. At 25℃ and 30℃, KS3, KS6, and KS8 showed higher biofilm-forming ability than S. aureus ATCC 29213. The antimicrobial resistance of the isolates was evaluated using the VITEK® 2 system; most isolates were resistant to marbofloxacin and nitrofurantoin (both 9/9, 100%), followed by enrofloxacin (7/9, 77.8%). Five of the nine isolates (5/9, 55.6%) showed multidrug resistance. Our study reports the abilities of K. salsicia to grow in the presence of high salt concentrations and at relatively low temperatures, along with its multidrug resistance and tendency to form biofilms.
Keywords
Kocuria salsicia; cheese brine; growth curve; biofilm; antimicrobial resistance;
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1 Barnes LM, Lo MF, Adams MR, Chamberlain AHL. 1999. Effect of milk proteins on adhesion of bacteria to stainless steel surfaces. Appl Environ Microbiol 65:4543-4548.   DOI
2 Becker K, Rutsch F, Uekotter A, Kipp F, Konig J, Marquardt T, Peters G, von Eiff C. 2008. Kocuria rhizophila adds to the emerging spectrum of micrococcal species involved in human infections. J Clin Microbiol 46:3537-3539.   DOI
3 Bintsis T, Papademas P. 2002. Microbiological quality of white-brined cheeses: A review. Int J Dairy Technol 55:113-120.   DOI
4 Clinical and Laboratory Standards Institute [CLSI]. 2020a. Performance standards for antimicrobial disk and dilution susceptibility tests for bacteria isolated from animals. 5th ed. CLSI, Wayne, PA, USA.
5 Clinical and Laboratory Standards Institute [CLSI]. 2020b. Performance standards for antimicrobial susceptibility testing. 30th ed. CLSI, Wayne, PA, USA.
6 de Jesus Pimentel-Filho N, de Freitas Martins MC, Nogueira GB, Mantovani HC, Vanetti MCD. 2014. Bovicin HC5 and nisin reduce Staphylococcus aureus adhesion to polystyrene and change the hydrophobicity profile and Gibbs free energy of adhesion. Int J Food Microbiol 190:1-8.   DOI
7 Di Ciccio P, Vergara A, Festino AR, Paludi D, Zanardi E, Ghidini S, Ianieri A. 2015. Biofilm formation by Staphylococcus aureus on food contact surfaces: Relationship with temperature and cell surface hydrophobicity. Food Control 50:930-936.   DOI
8 Golob M, Pate M, Kusar D, Dermota U, Avbersek J, Papic B, Zdovc I. 2019. Antimicrobial resistance and virulence genes in Enterococcus faecium and Enterococcus faecalis from humans and retail red meat. BioMed Res Int 2019:2815279.
9 Sohn KM, Baek JY, Kim SH, Cheon S, Kim YS. 2015. Catheter-related bacteremia caused by Kocuria salsicia: The first case. J Infect Chemother 21:305-307.   DOI
10 Soni I, Chakrapani H, Chopra S. 2015. Draft genome sequence of methicillin-sensitive Staphylococcus aureus ATCC 29213. Genome Announc 3:e01095-15.
11 Altuntas F, Yildiz O, Eser B, Gundogan K, Sumerkan B, Cetin M. 2004. Catheter-related bacteremia due to Kocuria rosea in a patient undergoing peripheral blood stem cell transplantation. BMC Infect Dis 4:1-3.   DOI
12 Banks MK, Bryers JD. 1991. Bacterial species dominance within a binary culture biofilm. Appl Environ Microbiol 57:1974-1979.   DOI
13 Kandi V, Palange P, Vaish R, Bhatti AB, Kale V, Kandi MR, Bhoomagiri MR. 2016. Emerging bacterial infection: Identification and clinical significance of Kocuria species. Cureus 8:e731.
14 Xu H, Zou Y, Lee HY, Ahn J. 2010. Effect of NaCl on the biofilm formation by foodborne pathogens. J Food Sci 75:M580-M585.   DOI
15 Lee JY, Kim SH, Jeong HS, Oh SH, Kim HR, Kim YH, Lee JN, Kook JK, Kho WG, Bae IK, Shin JH. 2009. Two cases of peritonitis caused by Kocuria marina in patients undergoing continuous ambulatory peritoneal dialysis. J Clin Microbiol 47:3376-3378.   DOI
16 Mehli L, Hoel S, Thomassen GMB, Jakobsen AN, Karlsen H. 2017. The prevalence, genetic diversity and antibiotic resistance of Staphylococcus aureus in milk, whey, and cheese from artisan farm dairies. Int Dairy J 65:20-27.   DOI
17 Rode TM, Langsrud S, Holck A, Moretro T. 2007. Different patterns of biofilm formation in Staphylococcus aureus under food-related stress conditions. Int J Food Microbiol 116:372-383.   DOI
18 Zwietering MH, Jongenburger I, Rombouts FM, Van't Riet K. 1990. Modeling of the bacterial growth curve. Appl Environ Microbiol 56:1875-1881.   DOI
19 Kim SB, Nedashkovskaya OI, Mikhailov VV, Han SK, Kim KO, Rhee MS, Bae KS. 2004. Kocuria marina sp. nov., a novel actinobacterium isolated from marine sediment. Int J Syst Evol Microbiol 54:1617-1620.   DOI
20 Jeong D, Kim DH, Song KY, Seo KH. 2018. Antimicrobial and anti-biofilm activities of Lactobacillus kefiranofaciens DD2 against oral pathogens. J Oral Microbiol 10:1472985.   DOI
21 Larson AE, Johnson EA, Nelson JH. 1999. Survival of Listeria monocytogenes in commercial cheese brines. J Dairy Sci 82:1860-1868.   DOI
22 Ingham SC, Su YC, Spangenberg DS. 2000. Survival of Salmonella typhimurium and Escherichia coli O157:H7 in cheese brines. Int J Food Microbiol 61:73-79.   DOI
23 Locatelli C, Cremonesi P, Bertocchi L, Zanoni MG, Barberio A, Drigo I, Varisco G, Castiglioni B, Bronzo V, Moroni P. 2016. Methicillin-resistant Staphylococcus aureus in bulk tank milk of dairy cows and effect of swine population density. J Dairy Sci 99:2151-2156.   DOI
24 McMahon DJ, Motawee MM, McManus WR. 2009. Influence of brine concentration and temperature on composition, microstructure, and yield of feta cheese. J Dairy Sci 92:4169-4179.   DOI
25 European Food Safety Authority, European Centre for Disease Prevention and Control. 2019. The European Union summary report on antimicrobial resistance in zoonotic and indicator bacteria from humans, animals and food in 2017. EFSA J 17:e05598.
26 Fox E, Hunt K, O'Brien M, Jordan K. 2011. Listeria monocytogenes in Irish Farmhouse cheese processing environments. Int J Food Microbiol 145:S39-S45.   DOI
27 Haastrup MK, Johansen P, Malskaer AH, Castro-Mejia JL, Kot W, Krych L, Arneborg N, Jespersen L. 2018. Cheese brines from Danish dairies reveal a complex microbiota comprising several halotolerant bacteria and yeasts. Int J Food Microbiol 285:173-187.   DOI
28 Savini V, Catavitello C, Masciarelli G, Astolfi D, Balbinot A, Bianco A, Febbo F, D'Amario C, D'Antonio D. 2010. Drug sensitivity and clinical impact of members of the genus Kocuria. J Med Microbiol 59:1395-1402.   DOI
29 Meletis G, Gogou V, Palamouti M, Spiropoulos P, Xanthopoulou K, Tantou P, Thomoglou V, Rizou A, Thomoglou V. 2012. Catheter-related relapsing peritonitis due to Kocuria varians in a patient undergoing continuous ambulatory peritoneal dialysis. Nefrologia (Madrid) 32:541-542.
30 Ryu JH, Beuchat LR. 2005. Biofilm formation by Escherichia coli O157:H7 on stainless steel: Effect of exopolysaccharide and Curli production on its resistance to chlorine. Appl Environ Microbiol 71:247-254.   DOI
31 Kang IB, Kim DH, Chon JW, Seo KH. 2018. Effect of microbial control measures on farmstead cheesemaking and antimicrobial resistance of Staphylococcus aureus and Enterococcus spp. isolates. J Food Saf 38:e12432.   DOI
32 Animal and Plant Quarantine Agency [APQA]. 2019. National antibiotic use and resistance monitoring. Available from: https://www.mfds.go.kr/brd/m_231/view.do?seq=33047&srchFr=&srchTo=&srchWord=&srchTp=&itm_seq_1=0&itm_seq_2=0&multi_itm_seq=0&company_cd=&company_nm=&page=1. Accessed at Oct 10, 2021.
33 Dunn R, Bares S, David MZ. 2011. Central venous catheter-related bacteremia caused by Kocuria kristinae: Case report and review of the literature. Ann Clin Microbiol Antimicrob 10:31.   DOI
34 Basaglia G, Carretto E, Barbarini D, Moras L, Scalone S, Marone P, De Paoli P. 2002. Catheter-related bacteremia due to Kocuria kristinae in a patient with ovarian cancer. J Clin Microbiol 40:311-313.   DOI
35 Bruins MJ, Juffer P, Wolfhagen MJ, Ruijs GJ. 2007. Salt tolerance of methicillin-resistant and methicillin-susceptible Staphylococcus aureus. J Clin Microbiol 45:682-683.   DOI
36 Moreira JS, Riccetto AGL, da Silva MTN, dos Santos Vilela MM. 2015. Endocarditis by Kocuria rosea in an immunocompetent child. Braz J Infect Dis 19:82-84.   DOI
37 Nilsson RE, Ross T, Bowman JP. 2011. Variability in biofilm production by Listeria monocytogenes correlated to strain origin and growth conditions. Int J Food Microbiol 150:14-24.   DOI
38 Purty S, Saranathan R, Prashanth K, Narayanan K, Asir J, Sheela Devi C, Kumar Amarnath S. 2013. The expanding spectrum of human infections caused by Kocuria species: A case report and literature review. Emerg Microbes Infect 2:1-8.
39 D'Amico DJ, Donnelly CW. 2008. Enhanced detection of Listeria spp. in farmstead cheese processing environments through dual primary enrichment, PCR, and molecular subtyping. J Food Prot 71:2239-2248.   DOI
40 Jang YS, Kim DH, Bae D, Kim SH, Kim H, Moon JS, Song KY, Chon JW, Seo KH. 2020. Prevalence, toxin-typing, and antimicrobial susceptibility of Clostridium perfringens from retail meats in Seoul, Korea. Anaerobe 64:102235.   DOI
41 Welch K, Cai Y, Stromme M. 2012. A method for quantitative determination of biofilm viability. J Funct Biomater 3:418-431.   DOI