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Acid Resistance of Non-O157 Shiga Toxin-Producing Escherichia coli Adapted in Fruit Juices in Simulated Gastric Fluid

위합성용액에서 과일주스에 노출한 Non-O157 Shiga Toxin-Producing Escherichia coli의 산 저항성 평가

  • Kim, Gwang-Hee (Department of Food Science and Biotechnology, Kangwon National University) ;
  • Oh, Deog-Hwan (Department of Food Science and Biotechnology, Kangwon National University)
  • 김광희 (강원대학교 식품생명공학과) ;
  • 오덕환 (강원대학교 식품생명공학과)
  • Received : 2015.12.23
  • Accepted : 2016.02.17
  • Published : 2016.04.30

Abstract

The objectives of this study were I) to compare the acid resistance (AR) of seven non-O157 Shiga toxin-producing Escherichia coli (STEC) serogroups, including O26, O45, O103, O111, O121, O145, and O157:H7 STEC isolated from various sources, in 400 mM acetic acid solution (AAS) at pH 3.2 and $30^{\circ}C$ for 25 min with or without glutamic acid and II) to determine strain survival upon exposure to simulated gastric fluid (SGF, pH 1.5) at $37^{\circ}C$ for 2 h after acid adaptation in apple, pineapple, orange, and strawberry juices at pH 3.8, $4^{\circ}C$ and $20^{\circ}C$. Results show that the O111 serogroup strains had the strongest AR (0.12 log reduction CFU/mL) which was very similar to that of O157:H7 STEC (P>0.05), compared to other serogroups in AAS without glutamic acid, whereas O26 serogroup strains showed the most sensitive AR. However, there was no significant (P>0.05) difference of AR among seven serogroups in AAS with glutamic acid. In the SGF study, 05-6545 (O45:H2), 08023 (O121:H19), and 03-4669 (O145:NM) strains adapted in fruit juices at $4^{\circ}C$ and $20^{\circ}C$ displayed enhanced survival with exposure to SGF for 60 min compared to 06E0218 (O157:H7) strains (P<0.05). In addition, 4 STEC strains adapted in pineapple juice at $4^{\circ}C$ showed enhanced survival with exposure to SGF for 60 min compared to those strains acid-adapted in the other fruit juices. Generally, adaptation at $4^{\circ}C$ in fruit juices resulted in significantly enhanced survival levels compared to acid-adapted at $20^{\circ}C$ and non-adapted conditions. The AR caused by adaptation in fruit juices at low temperature may thus increase survival of non-O157 STEC strain in acidic environments such as the gastrointestinal tract. These results suggest that more careful strategies should be provided to protect against risk of foodborne illness by non-O157 STEC.

References

  1. Parish ME, Narciso JA, Friedrich LM. 1997. Survival of Salmonellae in orange juice. J Food Saf 17: 273-281. https://doi.org/10.1111/j.1745-4565.1997.tb00194.x
  2. Yuk HG, Schneider KR. 2006. Adaptation of Salmonella spp. in juice stored under refrigerated and room temperature enhances acid resistance to simulated gastric fluid. Food Microbiol 23: 694-700. https://doi.org/10.1016/j.fm.2005.12.003
  3. Cody SH, Glynn MK, Farrar JA, Cairns KL, Griffin PM, Kobayashi J, Fyge M, Hoffman R, King AS, Lewis JH, Swaminathan B, Bryant RG, Vugia DJ. 1999. An outbreak of Escherichia coli O157:H7 infection from unpasteurized commercial apple juice. Ann Intern Med 130: 202-209. https://doi.org/10.7326/0003-4819-130-3-199902020-00005
  4. Besser RE, Lett SM, Weber JT, Doyle MP, Barrett TJ, Wells JG, Griffin PM. 1993. An outbreak of diarrhea and hemolytic uremic syndrome from Escherichia coli O157:H7 in fresh-pressed apple cider. JAMA 269: 2217-2220. https://doi.org/10.1001/jama.1993.03500170047032
  5. Vojdani JD, Beuchat LR, Tauxe RV. 2008. Juice-associated outbreaks of human illness in the United States, 1995 through 2005. J Food Prot 71: 356-364. https://doi.org/10.4315/0362-028X-71.2.356
  6. Scallan E, Hoekstra RM, Angulo FJ, Tauxe RV, Widdowson MA, Roy SL, Jones JL, Griffin PM. 2011. Foodborne illness acquired in the United States-major pathogens. Emerg Infect Dis 17: 7-15. https://doi.org/10.3201/eid1701.P11101
  7. Taylor EV, Nguyen TA, Machesky KD, Koch E, Sotir MJ, Bohm SR, Folster JP, Bokanyi R, Kupper A, Bidol SA, Emanuel A, Arends KD, Johnson SA, Dunn J, Stroika S, Patel MK, Williams I. 2013. Multistate outbreak of Escherichia coli O145 infections associated with romaine lettuce consumption, 2000. J Food Prot 76: 939-944. https://doi.org/10.4315/0362-028X.JFP-12-503
  8. Cheung MK, Li L, Nong W, Kwan HS. 2011. German Escherichia coli O104:H4 outbreak: whole-genome phylogeny without alignment. BMC Res Notes 4: 533. https://doi.org/10.1186/1756-0500-4-533
  9. Mellmann A, Harmsen D, Cummings CA, Zentz EB, Leopold SR, Rico A, Prior K, Szczepanowski R, Ji Y, Zhang W, McLaughlin SF, Henkhaus JK, Leopold B, Bielaszewska M, Prager R, Brzoska PM, Moore RL, Guenther S, Rothberg JM, Karch H. 2011. Prospective genomic characterization of the German enterohemorrhagic Escherichia coli O104:H4 outbreak by rapid next generation sequencing technology. PLoS ONE 6: e22751. https://doi.org/10.1371/journal.pone.0022751
  10. Kundsen DM, Yamamoto SA, Harris LJ. 2001. Survival of Salmonella spp. and Escherichia coli O157:H7 on fresh and frozen strawberries. J Food Prot 64: 1483-1488. https://doi.org/10.4315/0362-028X-64.10.1483
  11. Yu K, Newman MC, Archbold DD, Hamilton-Kemp TR. 2001. Survival of Escherichia coli O157:H7 on strawberry fruit and reduction of the pathogen population by chemical agents. J Food Prot 64: 1334-1340. https://doi.org/10.4315/0362-028X-64.9.1334
  12. Food and Drug Administration. 2001. Hazard Analysis and Critical Control Point (HACCP); Procedures for the safe and sanitary processing and importing of juice. Fed Regist 63: 6138-6202.
  13. Beuchat LR, Brackett RE. 1991. Behavior of Listeria monocytogenes inoculated into raw tomatoes and processed tomato products. Appl Environ Microbiol 57: 1367-1371.
  14. Miller LG, Kaspar CW. 1994. Escherichia coli O157:H7 acid tolerance and survival in apple cider. J Food Prot 57: 460-464. https://doi.org/10.4315/0362-028X-57.6.460
  15. Zhao T, Doyle MP, Besser RE. 1993. Fate of enterohemorrhagic Escherichia coli O157:H7 in apple cider with and without preservatives. Appl Environ Microbiol 59: 2526-2530.
  16. Oyarzabal OA, Nogueira MC, Gombas DE. 2003. Survival of Escherichia coli O157:H7, Listeria monocytogenes, and Salmonella in juice concentrates. J Food Prot 66: 1595-1598. https://doi.org/10.4315/0362-028X-66.9.1595
  17. Hsin-Yi C, Chou CC. 2001. Acid adaptation and temperature effect on the survival of E. coli O157:H7 in acidic fruit juice and lactic fermented milk product. Int J Food Microbiol 70: 189-195. https://doi.org/10.1016/S0168-1605(01)00538-4
  18. Smith JL. 2003. The role of gastric acid in preventing foodborne disease and how bacteria overcome acid conditions. J Food Prot 66: 1292-1303. https://doi.org/10.4315/0362-028X-66.7.1292
  19. Benjamin MM, Datta AR. 1995. Acid tolerance of enterohemorrhagic Escherichia coli. Appl Environ Microbiol 61: 1669-1672.
  20. Lin J, Smith MP, Chapin KC, Baik HS, Bennett GN, Foster JW. 1996. Mechanisms of acid resistance in enterohemorrhagic Escherichia coli. Appl Environ Microbiol 62: 3094-3100.
  21. Arnold KW, Kaspar CW. 1995. Starvation- and stationaryphase- induced acid tolerance in Escherichia coli O157:H7. Appl Environ Microbiol 61: 2037-2039.
  22. Murinda SE, Nguyen LT, Landers TL, Draughon FA, Mathew AG, Hogan JS, Smith KL, Hancock DD, Oliver SP. 2004. Comparison of Escherichia coli isolates from humans, food, and farm and companion animals for presence of Shiga toxin-producing E. coli virulence markers. Foodborne Pathog Dis 1: 178-184. https://doi.org/10.1089/fpd.2004.1.178
  23. Breidt F Jr, Hayes JS, McFeeters RF. 2004. Independent effects of acetic acid and pH on survival of Escherichia coli in simulated acidified pickle products. J Food Prot 67: 12-18. https://doi.org/10.4315/0362-028X-67.1.12
  24. Oh DH, Pan Y, Berry E, Cooley M, Mandrell R, Breidt F Jr. 2009. Escherichia coli O157:H7 strains isolated from environmental sources differ significantly in acetic acid resistance compared with human outbreak strains. J Food Prot 72: 503-509. https://doi.org/10.4315/0362-028X-72.3.503
  25. Beumer RD, de Vries J, Rombouts FM. 1992. Campylobacter jejuni non-culturable coccoid cells. Int J Food Microbiol 15: 153-163. https://doi.org/10.1016/0168-1605(92)90144-R
  26. King T, Lucchini S, Hinton JCD, Gobius K. 2010. Transcriptomic analysis of Escherichia coli O157:H7 and K-12 cultures exposed to inorganic and organic acids in stationary phase reveals acidulant- and strain-specific acid tolerance responses. Appl Environ Microbiol 76: 6514-6528. https://doi.org/10.1128/AEM.02392-09
  27. Lu HJ, Breidt F Jr, Perez-Diaz I. 2013. Development of an effective treatment for a 5-log reduction of Escherichia coli in refrigerated pickle products. J Food Sci 78: M264-M269. https://doi.org/10.1111/j.1750-3841.2012.02968.x
  28. Kalchayanand N, Arthur TM, Bosilevac JM, Schmidt JW, Wang R, Shackelford SD, Wheeler TL. 2012. Evaluation of commonly used antimicrobial interventions for fresh beef inoculated with Shiga toxin-producing Escherichia coli serotypes O26, O45, O103, O111, O121, O145, and O157:H7. J Food Prot 75: 1207-1212. https://doi.org/10.4315/0362-028X.JFP-11-531
  29. Buchanan RL, Edelson SG. 1999. pH-dependent stationaryphase acid resistance response of enterohemorrhagic Escherichia coli in the presence of various acidulants. J Food Prot 62: 211-218. https://doi.org/10.4315/0362-028X-62.3.211
  30. Comi G, Cocolin L, Manzano M, Cantoni C, Cattaneo M. 2000. Microorganisms behaviour in purposely contaminated fruit juices. Ind Bevande 167: 237-246.
  31. Brudzinski L, Harrison MA. 1998. Influence of incubation conditions on survival and acid tolerance response of Escherichia coli O157:H7 and non-O157:H7 isolates exposed to acetic acid. J Food Prot 61: 542-546. https://doi.org/10.4315/0362-028X-61.5.542
  32. Lin J, Lee IS, Frey J, Slonczewski JL, Foster JW. 1995. Comparative analysis of extreme acid survival in Salmonella typhimurium, Shigella flexneri, and Escherichia coli. J Bacteriol 177: 4097-4104. https://doi.org/10.1128/jb.177.14.4097-4104.1995
  33. Hersh BM, Farooq FT, Barstad DN, Blankenhorn DL, Slonczewski JL. 1996. A glutamate-dependent acid resistance gene in Escherichia coli. J Bacteriol 178: 3978-3981. https://doi.org/10.1128/jb.178.13.3978-3981.1996
  34. Richard HT, Foster JW. 2003. Acid resistance in Escherichia coli. Adv Appl Microbiol 52: 167-186. https://doi.org/10.1016/S0065-2164(03)01007-4
  35. Foster JW. 2004. Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol 2: 898-907. https://doi.org/10.1038/nrmicro1021
  36. Bhagwat AA, Chan L, Han R, Tan J, Kothary M, Jean- Gilles J, Tall BD. 2005. Characterization of enterohemorrhagic Escherichia coli strains based on acid resistance phenotypes. Infect Immun 73: 4993-5003. https://doi.org/10.1128/IAI.73.8.4993-5003.2005
  37. Kim GH, Breidt F, Fratamico P, Oh DH. 2015. Acid resistance and molecular characterization of Escherichia coli O157:H7 and different non-O157 Shiga toxin-producing E. coli serogroups. J Food Sci 80: M2257-M2264. https://doi.org/10.1111/1750-3841.12996
  38. Yuk HG, Marshall DL. 2005. Influence of acetic, citric, and lactic acids on Escherichia coli O157:H7 membrane lipid composition, verotoxin secretion, and acid resistance in simulated gastric fluid. J Food Prot 68: 673-679. https://doi.org/10.4315/0362-028X-68.4.673
  39. Buchanan RL, Edelson SG, Boyd G. 1999. Effects of pH and acid resistance on the radiation resistance of enterohemorrhagic Escherichia coli. J Food Prot 62: 219-228. https://doi.org/10.4315/0362-028X-62.3.219
  40. Han Y, Linton RH. 2004. Fate of Escherichia coli O157:H7 and Listeria monocytogenes in strawberry juice and acidified media at different pH values and temperatures. J Food Prot 67: 2443-2449. https://doi.org/10.4315/0362-028X-67.11.2443
  41. Smith JL, Fratamico PM. 2012. Effect of stress on non-O157 Shiga toxin-producing Escherichia coli. J Food Prot 75: 2241-2250. https://doi.org/10.4315/0362-028X.JFP-12-255
  42. Bergholz TM, Whittam TS. 2007. Variation in acid resistance among enterohaemorrhagic Escherichia coli in a simulated gastric environment. J Appl Microbiol 102: 352-362.
  43. Kim MR, Woo HC, Son WG. 2008. Survival of Listeria monocytogenes and Salmonella Typhimurium in retail mandarin orange, Prunus mume (maesil) and kiwi extracts. J Fd Hyg Safety 23: 62-67.