Journal of Food Hygiene and Safety (한국식품위생안전성학회지)

The Korean Society of Food Hygiene and Safety (한국식품위생안전성학회)
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Correlation Between food Processing-Associated Stress Tolerance and Antimicrobial Resistance in Food Pathogens

  • Woode, Benjamin Kojo (Institute of Food Science, University of Debrecen) ;
  • Daliri, Frank (Department of Agriculture Biotechnology, Kwame Nkrumah University of Science and Technology, Private Mail Bag, University Post Office) ;
  • Daliri, Eric Banan-Mwine (Department of Food Science and Biotechnology, Kangwon National University)
  • Received : 2020.02.07
  • Accepted : 2020.02.19
  • Published : 2020.04.30
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Abstract

Recently, consumer demand for safe but minimally processed food has rapidly increased. For this reason, many food processing industries are applying hurdle technology to enhance food safety, extend shelf life, and make foods appear minimally processed. Meanwhile, studies have shown that a treatment (stress) meant to inactivate foodborne pathogens may trigger adaptation mechanisms and could even offer cross protection against subsequent treatments. Also, certain routine farm practices such as antibiotic and herbicide use could result in the development of antibiotic-resistant pathogens. Such bacteria may be tolerant to food processing-associated stress and be more likely to remain viable in processed foods. In this review, we discuss the correlation between food processing-associated stress and antibiotic resistance. We also discuss molecular mechanisms such as the use of sigma factors, SOS response pathways and efflux pumps as means of cross protection against antimicrobial compounds and other food processing-associated stresses.

최근 최소한으로 가공된 안전한 식품에 대한 소비자의 수요가 기하급수적으로 증가하고 있다. 이러한 이유로 많은 식품가공 업체에서는 식품안전을 강화하고 유통기한을 연장하기 위한 최소한의 가공공정 중 허들기술(hurdle technology)을 적용하고 있다. 한편, 연구에 따르면 식품에 함유된 병원균을 비활성화하기 위한 공정 및 방법들은 식중독세균들의 스트레스 적응 메커니즘을 촉발시켜 심지어 후속 치료로 부터 교차 보호를 준다. 또한, 항생제와 제초제 사용과 같은 일상적인 농장 관행은 항생제 내성을 가진 병원균의 생성을 초래할 수 있다. 이러한 항생제 내성 박테리아는 식품 처리과정과 관련된 스트레스에 내성을 가질 수 있고 가공 식품에서 생존할 수 있는 가능성을 높일 수 있다. 이 리뷰에서는 식품가공과 관련된 스트레스와 항생제 내성의 상관관계에 대해 논의한다. 또한, 항균성 화합물 및 기타 식품 처리 관련 스트레스에 대한 교차 보호 수단으로서 시그마 인자(sigma factors), SOS 반응 경로(SOS response pathways) 및 유출 펌프(efflux pumps)의 사용과 같은 분자유전학적 기작에 대해서도 논의한다.

Keywords

References

  1. Yu, T., Jiang, X., Zhang, Y., Ji, S., Gao, W., Shi, L., Effect of benzalkonium chloride adaptation on sensitivity to antimicrobial agents and tolerance to environmental stresses in Listeria monocytogenes. Front. Microbiol.,9, 2906 (2018). https://doi.org/10.3389/fmicb.2018.02906
  2. Kurenbach, B., Hill, A.M., Godsoe, W., van Hamelsveld, S., Heinemann, J.A., Agrichemicals and antibiotics in combination increase antibiotic resistance evolution. PeerJ., 6, e5801 (2018). https://doi.org/10.7717/peerj.5801
  3. Aminov, R.I., A brief history of the antibiotic era: lessons learned and challenges for the future. Front. Microbiol., 1, 134 (2010). https://doi.org/10.3389/fmicb.2010.00134
  4. O'Neill, J., 2016, Tackling drug-resistant infections globally: Final report and recommendations. HM Government and Welcome Trust, UK.
  5. Liao, X., Ma, Y., Daliri, E. B. M., Koseki, S., Wei, S., Liu, D., Ye, X., Chen, S., Ding, T., Interplay of antibiotic resistance and food-associated stress tolerance in foodborne pathogens. Trends Food Sci Technol., 95, 97-106 (2019).
  6. Rasetti-Escargueil, C., Lemichez, E., Popoff, M.R., Public health risk associated with botulism as foodborne zoonoses. Toxins., 12(1), 17 (2020). https://doi.org/10.3390/toxins12010017
  7. Yuan, W., Tian, T., Yang, Q., Riaz, L., Transfer potentials of antibiotic resistance genes in Escherichia spp. strains from different sources. Chemosphere, 246, 125736 (2020). https://doi.org/10.1016/j.chemosphere.2019.125736
  8. Bag, S., Ghosh, T.S., Banerjee, S., Mehta, O., Verma, J., Dayal, M., Desigamani, A., Kumar, P., Saha, B., Kedia, S., Ahuja, V., Molecular insights into antimicrobial resistance traits of commensal human gut microbiota. Microb Ecol., 77(2), 546-57 (2019). https://doi.org/10.1007/s00248-018-1228-7
  9. Ma, Y., Lan, G., Li, C., Cambaza, E.M., Liu, D., Ye, X., Chen, S., Ding, T., Stress tolerance of Staphylococcus aureus with different antibiotic resistance profiles. Microb Pathogenesis., 133, 103549 (2019). https://doi.org/10.1016/j.micpath.2019.103549
  10. Bucur, F.I., Grigore-Gurgu, L., Crauwels, P., Riedel, C.U., Nicolau, A.I., Resistance of Listeria monocytogenes to stress conditions encountered in food and food processing environments. Front. Microbiol., 9, 2700 (2018). https://doi.org/10.3389/fmicb.2018.02700
  11. Zhang, C., Xu, L., Wang, X., Zhuang, K., Liu, Q., Effects of ultraviolet disinfection on antibiotic-resistant Escherichia coli from wastewater: Inactivation, antibiotic resistance profiles and antibiotic resistance genes. J. Appl. Microbiol., 123(1), 295-306 (2017). https://doi.org/10.1111/jam.13480
  12. Burgess, C.M., Gianotti, A., Gruzdev, N., Holah, J., Knochel, S., Lehner, A., Margas, E., Esser, S.S., Sela, S., Tresse, O., The response of foodborne pathogens to osmotic and desiccation stresses in the food chain. Int J Food Microbiol., 221, 37-53 (2016). https://doi.org/10.1016/j.ijfoodmicro.2015.12.014
  13. Komora, N., Bruschi, C., Magalhaes, R., Ferreira, V., Teixeira, P., Survival of Listeria monocytogenes with different antibiotic resistance patterns to food-associated stresses. Int. J. Food Microbiol., 245, 79-87 (2017). https://doi.org/10.1016/j.ijfoodmicro.2017.01.013
  14. Al-Nabulsi, A.A., Osaili, T.M., Shaker, R.R., Olaimat, A.N., Jaradat, Z.W., Elabedeen, N.A.Z., Holley, R.A., Effects of osmotic pressure, acid, or cold stresses on antibiotic susceptibility of Listeria monocytogenes. Food Microbiol., 46, 154-60 (2015). https://doi.org/10.1016/j.fm.2014.07.015
  15. Zhu, M., Dai, X., High salt cross-protects Escherichia coli from antibiotic treatment through increasing efflux pump expression. mSphere., 3(2), e00095-18 (2018).
  16. Jeong, D.-W., Heo, S., Lee, J.-H., Safety assessment of Tetragenococcus halophilus isolates from doenjang, a Korean high-salt-fermented soybean paste. Food Microbiol., 62, 92-98 (2017). https://doi.org/10.1016/j.fm.2016.10.012
  17. Liu, M., Li, Q., Sun, H., Jia, S., He, X., Li, M., Zhang, X.X., Ye, L., Impact of salinity on antibiotic resistance genes in wastewater treatment bioreactors. Chem. Eng. J., 338, 557-63 (2018). https://doi.org/10.1016/j.cej.2018.01.066
  18. Lado, B.H., Yousef, A.E., Alternative food-preservation technologies: efficacy and mechanisms. Microbes Infect., 4(4), 433-440 (2002). https://doi.org/10.1016/S1286-4579(02)01557-5
  19. Ebinesh, A., Vijaykumar, G., Kiran, T., Exposure to stress minimizes the zone of antimicrobial action: a phenotypic demonstration with six Acinetobacter baumannii strains. MicroMedicine., 6(1), 16-35 (2018).
  20. Rodriguez-Verdugo, A., Gaut, B.S., Tenaillon, O., Evolution of Escherichia coli rifampicin resistance in an antibiotic-free environment during thermal stress. BMC Evol. Biol., 13(1), 50 (2013). https://doi.org/10.1186/1471-2148-13-50
  21. McMahon, M.A.S., Xu, J., Moore, J.E., Blair, I.S., McDowell, D.A., Environmental stress and antibiotic resistance in food-related pathogens. Appl Environ Microbiol., 73(1), 211-217 (2007). https://doi.org/10.1128/AEM.00578-06
  22. Walsh, D., Sheridan, J., Duffy, G., Blair, I., McDowell, D., Harrington, D., Thermal resistance of wild-type and antibiotic-resistant Listeria monocytogenes in meat and potato substrates. J. Appl. Microbiol., 90(4), 555-560 (2001). https://doi.org/10.1046/j.1365-2672.2001.01284.x
  23. Doherty, A.M., Mcmahon, C.M., Sheridan, J., Blair, I., McDowell, D., Hegarty, T., Thermal resistance of Yersinia enterocolitica and Listeria monocytogenes in meat and potato substrates. J. Food Saf., 18(2), 69-83 (1998). https://doi.org/10.1111/j.1745-4565.1998.tb00204.x
  24. Duffy, G., Walsh, C., Blair, I., McDowell, D., Survival of antibiotic resistant and antibiotic sensitive strains of E. coli O157 and E. coli O26 in food matrices. Int J Food Microbiol 109(3), 179-186 (2006). https://doi.org/10.1016/j.ijfoodmicro.2006.01.024
  25. Miller, J., Novak, J., Knocke, W., Pruden, A., Elevation of antibiotic resistance genes at cold temperatures: implications for winter storage of sludge and biosolids. Lett Appl Microbiol., 59(6), 587-593 (2014). https://doi.org/10.1111/lam.12325
  26. Al-Nabulsi, A.A., Osaili, T.M., Elabedeen, N.A.Z., Jaradat, Z.W., Shaker, R.R., Kheirallah, K.A., Tarazi, Y.H., Holley, R.A., Impact of environmental stress desiccation, acidity, alkalinity, heat or cold on antibiotic susceptibility of Cronobacter sakazakii. Int. J. Food Microbiol., 146(2), 137-143 (2011). https://doi.org/10.1016/j.ijfoodmicro.2011.02.013
  27. De Sales, C.V., De Melo, A.N.F., Niedzwiedzka, K.M., De Souza, E.L., Schaffner, D.W., Magnani, M., Changes of antibiotic resistance phenotype in outbreak-linked Salmonella enterica strains after exposure to human simulated gastrointestinal conditions in chicken meat. J. Food Prot., 81(11), 1844-1850 (2018). https://doi.org/10.4315/0362-028X.JFP-18-213
  28. Bacon, R., Sofos, J., Kendall, P., Belk, K., Smith, G., Comparative analysis of acid resistance between susceptible and multi-antimicrobial-resistant Salmonella strains cultured under stationary-phase acid tolerance-inducing and noninducing conditions. J. Food Prot., 66(5), 732-740 (2003). https://doi.org/10.4315/0362-028X-66.5.732
  29. Mitosch, K., Rieckh, G., Bollenbach, T., Noisy response to antibiotic stress predicts subsequent single-cell survival in an acidic environment. Cell Syst., 4, 393-403 (2017). https://doi.org/10.1016/j.cels.2017.03.001
  30. Hughes, M., Yanamala, S., Francisco, M.S., Loneragan, G., Miller, M., Brashears, M., Reduction of multidrug-resistant and drug-susceptible Salmonella in ground beef and freshly harvested beef briskets after exposure to commonly used industry antimicrobial interventions. J. Food Prot., 73(7), 1231-1237 (2010). https://doi.org/10.4315/0362-028X-73.7.1231
  31. Cebrian, G., Sagarzazu, N., Aertsen, A., Pagan, R., Condon, S., Manas, P., Role of the alternative sigma factor ${\sigma}B$ on Staphylococcus aureus resistance to stresses of relevance to food preservation. J. Appl. Microbiol., 107(1), 187-196 (2009). https://doi.org/10.1111/j.1365-2672.2009.04194.x
  32. Boor, K.J., Bacterial stress responses: what doesn't kill them can make them stronger. PLoS biology., 4(1), e23 (2006). https://doi.org/10.1371/journal.pbio.0040023
  33. Browning, D.F., Busby, S.J., Local and global regulation of transcription initiation in bacteria. Nat. Rev. Microbiol, 14(10), 638 (2016). https://doi.org/10.1038/nrmicro.2016.103
  34. Schulthess, B., Meier, S., Homerova, D., Goerke, C., Wolz, C., Kormanec, J., Berger-Bachi, B., Bischoff, M., Functional characterization of the ${\sigma}B$-dependent yabJ-spoVG operon in Staphylococcus aureus: role in methicillin and glycopeptide resistance. Antimicrob. Agents Chemother., 53(5), 1832-1839 (2009). https://doi.org/10.1128/AAC.01255-08
  35. Kindrachuk, K.N., Fernandez, L., Bains, M., Hancock, R.E., Involvement of an ATP-dependent protease, PA0779/AsrA, in inducing heat shock in response to tobramycin in Pseudomonas aeruginosa. Antimicrob. Agents Chemother., 55(5), 1874-1882 (2011). https://doi.org/10.1128/AAC.00935-10
  36. Richard, H., Foster, J.W., Escherichia coli glutamate-and arginine-dependent acid resistance systems increase internal pH and reverse transmembrane potential. J Bacteriol., 186(18), 6032-6041 (2004). https://doi.org/10.1128/JB.186.18.6032-6041.2004
  37. Bojer, M.S., Frees, D., Ingmer, H., Sos, A., In Staphylococci: An addition to the paradigm of membrane-localized, SOSinduced cell division inhibition in bacteria. Curr. Genet., 1-5 (2020).
  38. Cirz, R.T., Jones, M.B., Gingles, N.A., Minogue, T.D., Jarrahi, B., Peterson, S.N., Romesberg, F.E., Complete and SOS-mediated response of Staphylococcus aureus to the antibiotic ciprofloxacin. J. bacterial., 189(2), 531-539 (2007). https://doi.org/10.1128/JB.01464-06
  39. Simmons, L.A., Foti, J.J., Cohen, S.E., Walker, G.C., The SOS regulatory network. EcoSal Plus., 2008 (2008).
  40. Gaupp, R., Ledala, N., Somerville, G.A., Staphylococcal response to oxidative stress. Front Cell Infect Microbiol., 2, 33 (2012).
  41. Erill, I., Campoy, S., Barbe, J., Aeons of distress: an evolutionary perspective on the bacterial SOS response. FEMS Microbiol. Rev., 31(6), 637-656 (2007). https://doi.org/10.1111/j.1574-6976.2007.00082.x
  42. Perez-Capilla, T., Baquero, M.-R., Gomez-Gomez, J.-M., Ionel, A., Martin, S., Blazquez, J., SOS-independent induction of dinB transcription by ${\beta}$-lactam-mediated inhibition of cell wall synthesis in Escherichia coli. J. Bacteriol., 187(4), 1515-1528 (2005). https://doi.org/10.1128/JB.187.4.1515-1518.2005
  43. Poole, K., Efflux pumps as antimicrobial resistance mechanisms. Ann. Med., 39(3), 162-176 (2007). https://doi.org/10.1080/07853890701195262
  44. Potenski, C.J., Gandhi, M., Matthews, K.R., Exposure of Salmonella Enteritidis to chlorine or food preservatives increases susceptibility to antibiotics. FEMS Microbiol Lett., 220(2), 181-186 (2003). https://doi.org/10.1016/S0378-1097(03)00099-5