Profiles of Non- Staphylococci in Retail Pork and Slaughterhouse Carcasses: Prevalence, Antimicrobial Resistance, and Genetic Determinant of Fusidic Acid Resistance

Overview

Journal Food Sci Anim Resour

Specialty Biotechnology

Date 2022 Mar 21

PMID 35310565

Authors

Yu Jin Yang

Gi Yong Lee

Sun Do Kim

Ji Heon Park

Soo In Lee

Geun-Bae Kim

Soo-Jin Yang

Affiliations

Soon will be listed here.

Abstract

As commensal colonizers in livestock, there has been little attention on staphylococci, especially non- staphylococci (NAS), contaminating meat production chain. To assess prevalence of staphylococci in retail pork and slaughterhouse carcass samples in Korea, we collected 578 samples from Korean slaughterhouses (n=311) and retail markets (n=267) for isolation of staphylococci and determined antimicrobial resistance phenotypes in all the isolates. The presence of and prevalence of -family genes (, , , and ) and mutations in genes were examined in fusidic acid resistant isolates. A total of 47 staphylococcal isolates of 4 different species ( n=4; , n=1; , n=10; , n=32) were isolated. Fusidic acid resistance were confirmed in 9/10 and all of the 32 (previously ) isolates. Acquired fusidic acid resistance genes were detected in all the resistant strains; and in and in . Multi-locus sequence type analysis revealed that ST63 (n=10, 31%) and ST30 (n=8, 25%) genotypes were most prevalent among fusidic acid resistant isolates. In conclusion, the high prevalence of -family genes in and strains isolated from pork indicated that NAS might act as a reservoir for fusidic acid resistance gene transmissions in pork production chains.

Citing Articles

Mammaliicoccus sciuri's Pan-Immune System and the Dynamics of Horizontal Gene Transfer Among Staphylococcaceae: a One-Health CRISPR Tale.

de Carvalho A, Giambiagi-deMarval M, Rossi C J Microbiol. 2024; 62(9):775-784.

PMID: 39037483 DOI: 10.1007/s12275-024-00156-7.

Study on the current research trends and future agenda in animal products: an Asian perspective.

Lee S, Lee D, Mariano E, Yun S, Lee J, Park J J Anim Sci Technol. 2024; 65(6):1124-1150.

PMID: 38616880 PMC: 11007299. DOI: 10.5187/jast.2023.e121.

Molecular characterization of non-aureus staphylococci and Mammaliicoccus from Hipposideros bats in Southwest Nigeria.

Adesoji T, George U, Sulayman T, Uwanibe J, Olawoye I, Igbokwe J Sci Rep. 2024; 14(1):6899.

PMID: 38519524 PMC: 10960025. DOI: 10.1038/s41598-024-57190-z.

Antimicrobial properties of strains for control of and strains, diarrhoea cause in weaning pigs.

Yoo Y, Lee J, Cho J, Yoon Y Vet Med (Praha). 2023; 68(5):191-199.

PMID: 37982025 PMC: 10581512. DOI: 10.17221/112/2022-VETMED.

Species Profiles and Antimicrobial Resistance of Non- Staphylococci Isolated from Healthy Broilers, Farm Environments, and Farm Workers.

Park J, Lee G, Lim J, Kim G, Park K, Yang S Food Sci Anim Resour. 2023; 43(5):792-804.

PMID: 37701746 PMC: 10493561. DOI: 10.5851/kosfa.2023.e36.

References

Kolbert C, Connolly J, Lee M, Persing D . Detection of the Staphylococcal mecA gene by chemiluminescent DNA hybridization. J Clin Microbiol. 1995; 33(8):2179-82. PMC: 228360. DOI: 10.1128/jcm.33.8.2179-2182.1995. View

Enright M, Day N, Davies C, Peacock S, Spratt B . Multilocus sequence typing for characterization of methicillin-resistant and methicillin-susceptible clones of Staphylococcus aureus. J Clin Microbiol. 2000; 38(3):1008-15. PMC: 86325. DOI: 10.1128/JCM.38.3.1008-1015.2000. View

Sugden R, Kelly R, Davies S . Combatting antimicrobial resistance globally. Nat Microbiol. 2016; 1(10):16187. DOI: 10.1038/nmicrobiol.2016.187. View

Tang Y, Larsen J, Kjeldgaard J, Andersen P, Skov R, Ingmer H . Methicillin-resistant and -susceptible Staphylococcus aureus from retail meat in Denmark. Int J Food Microbiol. 2017; 249:72-76. DOI: 10.1016/j.ijfoodmicro.2017.03.001. View

Hanson B, Dressler A, Harper A, Scheibel R, Wardyn S, Roberts L . Prevalence of Staphylococcus aureus and methicillin-resistant Staphylococcus aureus (MRSA) on retail meat in Iowa. J Infect Public Health. 2011; 4(4):169-74. DOI: 10.1016/j.jiph.2011.06.001. View

Hung W, Chen H, Lin Y, Tsai J, Chen C, Lu H . Skin Commensal Staphylococci May Act as Reservoir for Fusidic Acid Resistance Genes. PLoS One. 2015; 10(11):e0143106. PMC: 4651549. DOI: 10.1371/journal.pone.0143106. View

von Wintersdorff C, Penders J, van Niekerk J, Mills N, Majumder S, van Alphen L . Dissemination of Antimicrobial Resistance in Microbial Ecosystems through Horizontal Gene Transfer. Front Microbiol. 2016; 7:173. PMC: 4759269. DOI: 10.3389/fmicb.2016.00173. View

Wang Y, Lin Y, Wan T, Wang D, Lin H, Lin C . Distribution of antibiotic resistance genes among Staphylococcus species isolated from ready-to-eat foods. J Food Drug Anal. 2019; 27(4):841-848. PMC: 9306985. DOI: 10.1016/j.jfda.2019.05.003. View

Nemeghaire S, Argudin M, Haesebrouck F, Butaye P . Molecular epidemiology of methicillin-resistant Staphylococcus sciuri in healthy chickens. Vet Microbiol. 2014; 171(3-4):357-63. DOI: 10.1016/j.vetmic.2014.01.041. View

10.

ONeill A, McLaws F, Kahlmeter G, Henriksen A, Chopra I . Genetic basis of resistance to fusidic acid in staphylococci. Antimicrob Agents Chemother. 2007; 51(5):1737-40. PMC: 1855526. DOI: 10.1128/AAC.01542-06. View

11.

Turnidge J, Collignon P . Resistance to fusidic acid. Int J Antimicrob Agents. 1999; 12 Suppl 2:S35-44. DOI: 10.1016/s0924-8579(98)00072-7. View

12.

Ruppe E, Barbier F, Mesli Y, Maiga A, Cojocaru R, Benkhalfat M . Diversity of staphylococcal cassette chromosome mec structures in methicillin-resistant Staphylococcus epidermidis and Staphylococcus haemolyticus strains among outpatients from four countries. Antimicrob Agents Chemother. 2008; 53(2):442-9. PMC: 2630651. DOI: 10.1128/AAC.00724-08. View

13.

Fessler A, Billerbeck C, Kadlec K, Schwarz S . Identification and characterization of methicillin-resistant coagulase-negative staphylococci from bovine mastitis. J Antimicrob Chemother. 2010; 65(8):1576-82. DOI: 10.1093/jac/dkq172. View

14.

Godtfredsen W, JAHNSEN S, LORCK H, ROHOLT K, TYBRING L . Fusidic acid: a new antibiotic. Nature. 1962; 193:987. DOI: 10.1038/193987a0. View

15.

Okoli C, Njoga E, Enem S, Godwin E, Nwanta J, Chah K . Prevalence, toxigenic potential and antimicrobial susceptibility profile of isolated from ready-to-eat meats. Vet World. 2018; 11(9):1214-1221. PMC: 6200574. DOI: 10.14202/vetworld.2018.1214-1221. View

16.

Chuang Y, Huang Y . Livestock-associated meticillin-resistant Staphylococcus aureus in Asia: an emerging issue?. Int J Antimicrob Agents. 2015; 45(4):334-40. DOI: 10.1016/j.ijantimicag.2014.12.007. View

17.

Fijalkowski K, Peitler D, Karakulska J . Staphylococci isolated from ready-to-eat meat - Identification, antibiotic resistance and toxin gene profile. Int J Food Microbiol. 2016; 238:113-120. DOI: 10.1016/j.ijfoodmicro.2016.09.001. View

18.

McLaws F, Chopra I, ONeill A . High prevalence of resistance to fusidic acid in clinical isolates of Staphylococcus epidermidis. J Antimicrob Chemother. 2008; 61(5):1040-3. DOI: 10.1093/jac/dkn071. View

19.

Wu S, Huang J, Wu Q, Zhang J, Zhang F, Yang X . Isolated From Retail Meat and Meat Products in China: Incidence, Antibiotic Resistance and Genetic Diversity. Front Microbiol. 2018; 9:2767. PMC: 6249422. DOI: 10.3389/fmicb.2018.02767. View

20.

Huber H, Ziegler D, Pfluger V, Vogel G, Zweifel C, Stephan R . Prevalence and characteristics of methicillin-resistant coagulase-negative staphylococci from livestock, chicken carcasses, bulk tank milk, minced meat, and contact persons. BMC Vet Res. 2011; 7:6. PMC: 3042402. DOI: 10.1186/1746-6148-7-6. View