Browse > Article
http://dx.doi.org/10.13103/JFHS.2020.35.4.391

Biofilm Formation, Antimicrobial Peptide Resistance, and Hydrogen Peroxide Resistance in Livestock-Associated Staphylococcus aureus Isolates  

Lee, Gi Yong (Department of Animal Science and Technology, Chung-Ang University)
Kim, Sun Do (Department of Animal Science and Technology, Chung-Ang University)
Yang, Soo-Jin (Department of Animal Science and Technology, Chung-Ang University)
Publication Information
Journal of Food Hygiene and Safety / v.35, no.4, 2020 , pp. 391-397 More about this Journal
Abstract
Human infections with livestock-associated methicillin-resistant/-susceptible Staphylococcus aureus (LA-MRSA/LA-MSSA) have recently been increasing significantly. These LA-MRSA and LA-MSSA strains can be transmitted to individuals who have frequent contact with livestock animals and foods of animal origin. In this study, major virulence potentials of S. aureus such as biofilm formation, antimicrobial peptide resistance, and in vitro hydrogen peroxide (H2O2) resistance were assessed using 20 MRSA and MSSA strains isolated from raw milk, beef cattle, and workers in the livestock industry. Static biofilm formation assays revealed that there is no difference in levels of biofilm production between MRSA versus MSSA or bovine- versus human-associated strains. In vitro BMAP (bovine myeloid antimicrobial peptide)-28 susceptibility assays also revealed no difference in the resistance to the antimicrobial peptide between MRSA versus MSSA or bovine- versus human-associated S. aureus strains. However, LA-MRSA strains displayed increased resistance to H2O2, which may play an important role in survival and dissemination of the pathogen in livestock. These results provide an important basis for understanding pathogenic potentials of LA-MRSA and LA-MSSA strains in human and animal hosts.
Keywords
Staphylococcus aureus; Biofilm; Antimicrobial peptide resistance; Hydrogen peroxide resistance;
Citations & Related Records
Times Cited By KSCI : 2  (Citation Analysis)
연도 인용수 순위
1 Okuma, K., Iwakawa, K., Turnidge, J.D., Grubb, W.B., Bell, J.M., O'Brien, F.G., Dissemination of new methicillin-resistant Staphylococcus aureus clones in the community. J. Clin. Microbiol., 40(11), 4289-94 (2002).   DOI
2 Naimi, T.S., LeDell, K.H., Como-Sabetti, K., Borchardt, S.M., Boxrud, D.J., Etienne, J., Comparison of communityand health care-associated methicillin-resistant Staphylococcus aureus infection. JAMA, 290(22), 2976-84 (2003).   DOI
3 Back, S.H., Eom, H.S., Lee, H.H., Lee, G.Y., Park, K.T., Yang, S.J., Livestock-associated methicillin-resistant Staphylococcus aureus in Korea: antimicrobial resistance and molecular characteristics of LA-MRSA strains isolated from pigs, pig farmers, and farm environment. J. Vet. Sci., 21(1), e2 (2020).   DOI
4 Eom, H.S., Back, S.H., Lee, H.H., Lee, G.Y., Yang, S.J., Prevalence and characteristics of livestock-associated methicillin- susceptible Staphylococcus aureus in the pork production chain in Korea. J. Vet. Sci., 20(6), e69 (2019).   DOI
5 Vincze, S., Brandenburg, A.G., Espelage, W., Stamm, I., Wieler, L.H., Kopp, P.A., Risk factors for MRSA infection in companion animals: results from a case-control study within Germany. Int. J. Med. Microbiol., 304(7), 787-93 (2014).   DOI
6 Moon, D.C., Jeong, S.K., Hyun, B.H., Lim, S.K., Prevalence and characteristics of methicillin-resistant Staphylococcus aureus Isolates in pigs and pig farmers in Korea. Foodborne Pathog Dis., 16(4), 256-61 (2019).   DOI
7 Zhang, Y., Wang, Y., Cai, R., Shi, L., Li, C., Yan, H., Prevalence of enterotoxin genes in Staphylococcus aureus isolates from pork production. Foodborne Pathog Dis., 15(7), 437-43 (2018).   DOI
8 Moon, D.C., Tamang, M.D., Nam, H.M., Jeong, J.H., Jang, G.C., Jung, S.C., Identification of livestock-associated methicillin- resistant Staphylococcus aureus isolates in Korea and molecular comparison between isolates from animal carcasses and slaughterhouse workers. Foodborne Pathog Dis., 12(4), 327-34 (2015).   DOI
9 Kim, Y.B., Seo, K.W., Jeon, H.Y., Lim, S.K., Lee, Y.J., Characteristics of the antimicrobial resistance of Staphylococcus aureus isolated from chicken meat produced by different integrated broiler operations in Korea. Poult Sci., 97(3), 962-9 (2018).   DOI
10 Osman, K.M., Amer, A.M., Badr, J.M., Saad, A.S., Prevalence and antimicrobial resistance profile of Staphylococcus species in chicken and beef raw meat in Egypt. Foodborne Pathog Dis., 12(5), 406-13 (2015).   DOI
11 Song, J.W., Yang, S.J., Shin, S., Seo, K.S., Park, Y.H., Park, K.T., Genotypic and phenotypic characterization of methicillin-resistant Staphylococcus aureus isolated from bovine mastitic milk in Korea. J. Food Prot., 79(10), 1725-32 (2016).   DOI
12 Pirolo, M., Visaggio, D., Gioffre, A., Artuso, I., Gherardi, M., Pavia, G., Unidirectional animal-to-human transmission of methicillin-resistant Staphylococcus aureus ST398 in pig farming; evidence from a surveillance study in southern Italy. Antimicrob Resist Infect Control., 8, 187 (2019).   DOI
13 Lee, H.H., Lee, G.Y., Eom, H.S., Yang, S.J., Occurrence and characteristics of methicillin-resistant and -susceptible Staphylococcus aureus isolated from the beef production chain in Korea. Food Sci. Anim. Resour., 40(3), 401-14 (2020).   DOI
14 Price, L.B., Stegger, M., Hasman, H., Aziz, M., Larsen, J., Andersen, P.S., Staphylococcus aureus CC398: host adaptation and emergence of methicillin resistance in livestock. MBio., 3(1), e00305-11 (2012).
15 Schijffelen, M.J., Boel, C.H., van Strijp, J.A., Fluit, A.C., Whole genome analysis of a livestock-associated methicillin- resistant Staphylococcus aureus ST398 isolate from a case of human endocarditis. BMC Genomics., 11, 376 (2010).   DOI
16 He, L., Zheng, H.X., Wang, Y., Le, K.Y., Liu, Q., Shang, J., Detection and analysis of methicillin-resistant humanadapted sequence type 398 allows insight into communityassociated methicillin-resistant Staphylococcus aureus evolution. Genome Med., 10(1), 5 (2018).   DOI
17 Smith, T.C., Male, M.J., Harper, A.L., Kroeger, J.S., Tinkler, G.P., Moritz, E.D., Methicillin-resistant Staphylococcus aureus (MRSA) strain ST398 is present in midwestern U.S. swine and swine workers. PLoS One., 4(1), e4258 (2009).   DOI
18 Pompilio, A., De Nicola, S., Crocetta, V., Guarnieri, S., Savini, V., Carretto, E., New insights in Staphylococcus pseudintermedius pathogenicity: antibiotic-resistant biofilm formation by a human wound-associated strain. BMC Microbiol., 15, 109 (2015).   DOI
19 Giacometti, A., Cirioni, O., Ghiselli, R., Bergnach, C., Orlando, F., D'Amato, G., The antimicrobial peptide BMAP- 28 reduces lethality in mouse models of staphylococcal sepsis. Crit Care Med., 32(12), 2485-90 (2004).   DOI
20 Takagi, S., Hayashi, S., Takahashi, K., Isogai, H., Bai, L., Yoneyama, H., Antimicrobial activity of a bovine myeloid antimicrobial peptide (BMAP-28) against methicillin-susceptible and methicillin-resistant Staphylococcus aureus. Anim. Sci. J., 83(6), 482-6 (2012).   DOI
21 Xiong, Y.Q., Mukhopadhyay, K., Yeaman, M.R., Adler- Moore, J., Bayer, A.S., Functional interrelationships between cell membrane and cell wall in antimicrobial peptide- mediated killing of Staphylococcus aureus. Antimicrob Agents Chemother, 49(8), 3114-21 (2005).   DOI
22 Liu, G.Y., Essex, A., Buchanan, J.T., Datta, V., Hoffman, H.M., Bastian, J.F., Staphylococcus aureus golden pigment impairs neutrophil killing and promotes virulence through its antioxidant activity. J. Exp. Med., 202(2), 209-15 (2005).   DOI
23 Mama, O.M., Morales, L., Ruiz-Ripa, L., Zarazaga, M., Torres, C., High prevalence of multidrug resistant S. aureus- CC398 and frequent detection of enterotoxin genes among non-CC398 S. aureus from pig-derived food in Spain. Int. J. Food Microbiol., 320, 108510 (2020).   DOI
24 Sieber, R.N., Skov, R.L., Nielsen, J., Schulz, J., Price, L.B., Aarestrup, F.M., Drivers and dynamics of methicillin-resistant livestock-associated Staphylococcus aureus CC398 in pigs and humans in Denmark. Mbio., 9(6), e02142-18 (2018).
25 Iqbal, Z., Seleem, M.N., Hussain, H.I., Huang, L., Hao, H., Yuan, Z., Comparative virulence studies and transcriptome analysis of Staphylococcus aureus strains isolated from animals. Sci. Rep., 6, 35442 (2016).   DOI
26 Archer, N.K., Mazaitis, M.J., Costerton, J.W., Leid, J.G., Powers, M.E., Shirtliff, M.E., Staphylococcus aureus biofilms: properties, regulation, and roles in human disease. Virulence, 2(5), 445-59 (2011).   DOI
27 Abdalrahman, L.S., Stanley, A., Wells, H., Fakhr, M.K., Isolation, virulence, and antimicrobial resistance of methicillinresistant Staphylococcus aureus (MRSA) and methicillin sensitive Staphylococcus aureus (MSSA) strains from Oklahoma retail poultry meats. Int. J. Environ. Res. Public Health, 12(6), 6148-61 (2015).   DOI
28 Randad, P.R., Dillen, C.A., Ortines, R.V., Mohr, D., Aziz, M., Price, L.B., Comparison of livestock-associated and community-associated Staphylococcus aureus pathogenicity in a mouse model of skin and soft tissue infection. Sci. Rep., 9(1), 6774 (2019).   DOI
29 Sanchez, C.J., Jr. Mende, K., Beckius, M.L., Akers, K.S., Romano, D.R., Wenke, J.C., Biofilm formation by clinical isolates and the implications in chronic infections. BMC Infect Dis., 13, 47 (2013).   DOI
30 Neopane, P., Nepal, H.P., Shrestha, R., Uehara, O., Abiko, Y., In vitro biofilm formation by Staphylococcus aureus isolated from wounds of hospital-admitted patients and their association with antimicrobial resistance. Int. J. Gen. Med., 11, 25-32 (2018).   DOI
31 Thurlow, L.R., Hanke, M.L., Fritz, T., Angle, A., Aldrich, A., Williams, S.H., Staphylococcus aureus biofilms prevent macrophage phagocytosis and attenuate inflammation in vivo. J. Immunol., 186(11), 6585-96 (2011).   DOI
32 Srey, S., Jahid, I.K., Ha, S.D., Biofilm formation in food industries: A food safety concern. Food Control., 31(2), 572-85 (2013).   DOI
33 Peschel, A., Collins, L.V., Staphylococcal resistance to antimicrobial peptides of mammalian and bacterial origin. Peptides, 22(10),1651-9 (2001).   DOI
34 Stefanetti, V., Bietta, A., Pascucci, L., Marenzoni, M.L., Coletti, M., Franciosini, M.P., Investigation of the antibiotic resistance and biofilm formation of Staphylococcus pseudintermedius strains isolated from canine pyoderma. Vet Ital., 53(4), 289-96 (2017).
35 McCarthy, H., Rudkin, J.K., Black, N.S., Gallagher, L., O'Neill, E., O'Gara, J.P., Methicillin resistance and the biofilm phenotype in Staphylococcus aureus. Front Cell Infect Microbiol., 5, 1 (2015).   DOI
36 Scheenstra, M.R., van den Belt M., Tjeerdsma-van Bokhoven, J.L.M., Schneider, V.A.F., Ordonez, S.R., van Dijk, A., Cathelicidins PMAP-36, LL-37 and CATH-2 are similar peptides with different modes of action. Sci. Rep., 9(1), 4780 (2019).   DOI
37 Ernst, C.M., Staubitz, P., Mishra, N.N., Yang, S.J., Hornig, G., Kalbacher, H., The bacterial defensin resistance protein MprF consists of separable domains for lipid lysinylation and antimicrobial peptide repulsion. PLoS Pathog., 5(11), e1000660 (2009).   DOI
38 Peschel, A., Jack, R.W., Otto, M., Collins, L.V., Staubitz, P., Nicholson, G., Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J Exp Med. 193(9), 1067-76 (2001).   DOI
39 Buchan, K.D., Foster, S.J., Renshaw, S.A., Staphylococcus aureus: setting its sights on the human innate immune system. Microbiology. 165(4), 367-85 (2019).   DOI
40 Rowe, S.E., Wagner, N.J., Li, L., Beam, J.E., Wilkinson, A.D., Radlinski, L.C., Reactive oxygen species induce antibiotic tolerance during systemic Staphylococcus aureus infection. Nat. Microbiol., 5(2), 282-90 (2020).   DOI
41 Amenu, K., Grace, D., Nemo, S., Wieland, B., Bacteriological quality and safety of ready-to-consume milk and naturally fermented milk in Borana pastoral area, southern Ethiopia. Trop Anim Health Prod., 51(7), 2079-84 (2019).   DOI
42 Turner, N.A., Sharma-Kuinkel, B.K., Maskarinec, S.A., Eichenberger, E.M., Shah, P.P., Carugati, M., Methicillinresistant Staphylococcus aureus: an overview of basic and clinical research. Nat. Rev. Microbiol., 17(4), 203-18 (2019).   DOI