Browse > Article
http://dx.doi.org/10.4014/jmb.1707.07041

Correlation between Changes in Microbial/Physicochemical Properties and Persistence of Human Norovirus during Cabbage Kimchi Fermentation  

Lee, Hee-Min (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Lee, Ji-Hyun (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Kim, Sung Hyun (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Yoon, So-Ra (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Lee, Jae Yong (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Ha, Ji-Hyoung (Hygienic Safety and Analysis Center, World Institute of Kimchi)
Publication Information
Journal of Microbiology and Biotechnology / v.27, no.11, 2017 , pp. 2019-2027 More about this Journal
Abstract
Recently, cabbage kimchi has occasionally been associated with the foodborne diseases of enteric viruses such as human norovirus (HuNoV). This study aimed to evaluate the correlation between microbial/physicochemical properties and persistence of HuNoV in experimentally contaminated cabbage kimchi fermented and stored at $4^{\circ}C$ or $10^{\circ}C$ for 28 days. Changes in organic acid content, lactic acid bacteria (LAB), acidity, pH, and salinity were analyzed. The recovery of structurally intact HuNoV was examined for up to 28 days post-inoculation, using a NoV GII.4 monoclonal antibody-conjugated immuno-magnetic separation method combined with quantitative real-time reverse transcription polymerase chain reaction. On day 0, LAB loads were $4.70log_{10}$ colony forming units/g and HuNoV GII.4 titers were $2.57log_{10}\;genomic\;copies/{\mu}l$, at both temperatures. After 28 days, intact HuNoV titers decreased to 1.58 ($4^{\circ}C$) and $1.04(10^{\circ}C)log_{10}\;genomic\;copies/{\mu}l$, whereas the LAB density increased. This correlated with a gradual increase in lactic acid and acetic acid at both temperatures. Our findings support a statistical correlation between changes in physicochemical properties and the recovery of structurally intact HuNoV GII.4. Moreover, we determined that the production of organic acid and low pH could affect HuNoV GII.4 titers in cabbage kimchi during fermentation. However, HuNoV GII.4 was not completely eliminated by microbial/physicochemical factors during fermentation, although HuNoV GII.4 was reduced. Based on this, we speculate that the persistence of HuNoV GII.4 may be affected by the continually changing conditions during kimchi fermentation.
Keywords
Cabbage kimchi; detection; fermentation; human norovirus; lactic acid bacteria; organic acid;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
연도 인용수 순위
1 Coleman DJ, Chick KE, Nye KJ. 1995. An evaluation of immunomagnetic separation for the detection of salmonellas in raw chicken carcasses. Lett. Appl. Microbiol. 21: 152-154.   DOI
2 Tian P, Engelbrektson A, Mandrell R. 2008. Two-log increase in sensitivity for detection of norovirus in complex samples by concentration with porcine gastric mucin conjugated to magnetic beads. Appl. Environ. Microbiol. 74: 4271-4276.   DOI
3 Morton V, Jean J, Farber J, Mattison K. 2009. Detection of noroviruses in ready-to-eat foods by using carbohydrate-coated magnetic beads. Appl. Environ. Microbiol. 75: 4641-4643.   DOI
4 Pan L, Zhang Q, Li X, Tian P. 2012. Detection of human norovirus in cherry tomatoes, blueberries and vegetable salad by using a receptor-binding capture and magnetic sequestration (RBCMS) method. Food Microbiol. 30: 420-426.   DOI
5 Cho Y, Rhee HS. 1991. Effect of lactic acid bacteria and temperature on kimchi fermentation (II). Korean J. Food Cook. Sci. 7: 89-95.
6 Daniels NA, Bergmire-Sweat DA, Schwab KJ, Hendricks KA, Reddy S, Rowe SM, et al. 2000. A foodborne outbreak of gastroenteritis associated with Norwalk-like viruses: first molecular traceback to deli sandwiches contaminated during preparation. J. Infect. Dis. 181: 1467-1470.   DOI
7 Guevremont E, Brassard J, Houde A, Simard C, Trottier YL. 2006. Development of an extraction and concentration procedure and comparison of RT-PCR primer systems for the detection of hepatitis A virus and norovirus GII in green onions. J. Virol. Methods 134: 130-135.   DOI
8 Hutin YJ, Pool V, Cramer EH, Nainanm OV, Weth J, Williams IT, et al. 1999. A multistate, foodborne outbreak of hepatitis A. N. Engl. J. Med. 340: 595-602.   DOI
9 Le Guyader F, Dubois E, Menard D, Pommepuy M. 1994. Detection of hepatitis A virus, rotavirus, and enterovirus on naturally contaminated shellfish and sediment by reverse transcription-seminested PCR. Appl. Environ. Microbiol. 60:3665-3671.
10 Potasman I, Paz A, Odeh M. 2002. Infectious outbreaks associated with bivalve shellfish consumption: a worldwide perspective. Clin. Infect. Dis. 35: 921-928.   DOI
11 Rosenblum LS, Mirkin IR, Allen DT, Safford D, Hadler SC. 1990. A multifocal outbreak of hepatitis A traced to commercially distributed lettuce. Am. J. Public Health 80: 1075-1080.   DOI
12 Rutjes SA, Lodder-Verschoor F, van der Poel WH, van Duijoven YT, de Roda Husman AM. 2006. Detection of noroviruses in foods: a study on virus extraction procedures in foods implicated in outbreaks of human gastroenteritis. J. Food Prot. 69: 1949-1956.   DOI
13 Shin SB, Oh EG, Yu H, Lee HJ, Kim JH, Park K, et al. 2010. Inactivation of a norovirus surrogate (feline calicivirus) during the ripening of oyster kimchi. Korean J. Fish. Aquat. Sci. 43: 415-420.
14 Charenjiratragul W, Bhoopong P, Kantachote D, Jomduang S, Kong-Ngoen R, Nair GB, et al. 2010. Inhibitory activity of lactic acid bacteria isolated from Thai fermented food against pandemic strains of Vibrio parahaemolyticus. J. Food Saf. 30: 67-82.   DOI
15 Hernandez D, Cardell E, Zarate V. 2005. Antimicrobial activity of lactic acid bacteria isolated from Tenerife cheese:initial characterization of plantaricin TF711, a bacteriocinlike substance produced by Lactobacillus plantarum TF711. J. Appl. Microbiol. 99: 77-84.   DOI
16 Gagne MJ, Barrette J, Savard T, Brassard J. 2015. Evaluation of survival of murine norovirus-1 during sauerkraut fermentation and storage under standard and low-sodium conditions. Food Microbiol. 52: 119-123.   DOI
17 Lindesmith L, Moe C, Marionneau S, Ruvoen N, Jiang X, Lindblad L, et al. 2003. Human susceptibility and resistance to Norwalk virus infection. Nat. Med. 9: 548-553.   DOI
18 Lai CC, Wang YH, Wu CY, Hung CH, Jiang DDS, Wu FT. 2013. A norovirus outbreak in a nursing home: norovirus shedding time associated with age. J. Clin. Virol. 56: 96-101.   DOI
19 Lim MY, Kim JM, Ko GP. 2010. Disinfection kinetics of murine norovirus using chlorine and chlorine dioxide. Water Res. 44: 3243-3251.   DOI
20 Siebenga JJ, Vennema H, Zheng DP, Vinje J, Lee BE, Pang XL, et al. 2009. Norovirus illness is a global problem: emergence and spread of norovirus GII. 4 variants, 2001-2007. J. Infect. Dis. 200: 802-812.   DOI
21 Patel MM, Widdowson MA, Glass RI, Akazawa K, Vinje J, Parashar UD. 2008. Systematic literature review of role of noroviruses in sporadic gastroenteritis. Emerg. Infect. Dis. 14: 1224-1231.   DOI
22 van Asten L, Siebenga J, van den Wijngaard C, Verheij R, van Vliet H, Kretzschmar M, et al. 2011. Unspecified gastroenteritis illness and deaths in the elderly associated with norovirus epidemics. Epidemiology 22: 336-343.   DOI
23 Poschetto LF, Ike A, Papp T, Mohn U, Bohm R, Marschang RE. 2007. Comparison of the sensitivities of noroviruses and feline calicivirus to chemical disinfection under field-like conditions. Appl. Environ. microbiol. 73: 5494-5500.   DOI
24 Berger CN, Sodha SV, Shaw RK, Griffin PM, Pink D, Hand P, et al. 2010. Fresh fruit and vegetables as vehicles for the transmission of human pathogens. Environ. Microbiol. 12:2385-2397.   DOI
25 Doyle MP, Erickson MC. 2008. Summer meeting 2007 - the problems with fresh produce: an overview. J. Appl. Microbiol. 105: 317-330.   DOI
26 Salkind NJ. 2016. Statistics for people who (think they) hate statistics: Using microsoft excel 2016, pp. 129. 4th Ed. sage publications, Los Angeles, California.
27 Hansman GS, Shahzad-Ul-Hussan S, McLellan JS, Chuang GY, Georgiev I, Shimoike T, et al. 2012. Structural basis for norovirus inhibition and fucose mimicry by citrate. J. Virol. 86: 284-292.   DOI
28 Pavlova NI, Savinova OV, Nikolaeva SN, Boreko EI, Flekhter OB. 2003. Antiviral activity of botulin, betulinic and betulonic acids against some enveloped and non-enveloped viruses. Fitoterapia 74: 489-492.   DOI
29 Croci L, Medici D, Scalfaro C, Fiore A, Toti L. 2002. The survival of hepatitis A virus in fresh produce. Int. J. Food Microbiol. 73: 29-34.   DOI
30 Kukavica-Ibrilj I, Darveau A, Jean J, Fliss I. 2004. Heptitis A virus attachment to agri-food surfaces using immunological and thermodynamic assays. J. Appl. Microbiol. 97: 923-934.   DOI
31 Lee MJ, Kim WH, Cho HG, Lee SS. 2012. Epidemiological study of ground waterborne norovirus GI.3-associated gastroenteritis outbreaks in Gyeonggi province of South Korea in May 2011. J. Bacteriol. Virol. 42: 232-241.   DOI
32 Park JH, Jung S, Shin JS, Lee JS, Joo IS, Lee DY. 2015. Three gastroenteritis outbreaks in South Korea caused by consumption of kimchi tainted by norovirus GI. 4. Foodborne Pathog. Dis. 12: 221-227.   DOI
33 Kim MJ, Kim KS. 2014. Tyramine production among lactic acid bacteria and other species isolated from kimchi. Lebensm. Wiss. Technol. 56: 406-413.   DOI
34 Inatsu Y, Bari ML, Kawasaki S, Isshiki K. 2004. Survival of Escherichia coli O157:H7, Salmonella enteritidis, Staphylococcus aureus, and Listeria monocytogenes in kimchi. J. Food Prot. 67: 1497-1500.   DOI
35 Tamang JP, Shin DH, Jung SJ, Chae SW. 2016. Functional Properties of microorganisms in fermented foods. Front. Microbiol. 7: 578.
36 Hewitt J, Greening GE. 2004. Survival and persistence of norovirus, hepatitis A virus, and feline calicivirus in marinated mussels. J. Food Prot. 67: 1743-1750.   DOI
37 Cho GY, Lee MH, Choi C. 2011. Survival of Escherichia coli O157:H7 and Listeria monocytogenes during kimchi fermentation supplemented with raw pork meat. Food Control 22: 1253-1260.   DOI
38 Sheo HJ, Seo YS. 2003. The antibacterial action of Chinese cabbage kimchi juice on Staphylococcus aureus, Salmonella enteritidis, Vibrio parahaemolyticus and Enterobacter cloacae. J. Korean Soc. Food Sci. Nutr. 32: 1351-1356.   DOI
39 Kang CH, Chung KO, Ha DM. 2002. Inhibitory effect on the growth of intestinal pathogenic bacteria by kimchi fermentation. Korean J. Food Sci. Technol. 34: 480-486.
40 Cannon JL, Papafragkou E, Park GW, Osborne J, Jaykus LA, Vinje J. 2006. Surrogates for the study of norovirus stability and inactivation in the environment: a comparison of murine norovirus and feline calicivirus. J. Food Prot. 69: 2761-2765.   DOI
41 Mheen TI, Kwon TW, Lee CH. 1981. Traditional fermented food products in Korea. Microbiol. Biotechnol. Lett. 9: 253-261.
42 Mheen TI, Kwon TW. 1984. Effect of temperature and salt concentration on kimchi fermentation. Kor. J. Food Sci. Technol. 16: 443-450.
43 Park WS, Lee IS, Han YS, Koo YJ. 1994. Kimchi preparation with brined Chinese cabbage and seasoning mixture stored separately. Korean J. Food Sci. Technol. 26: 231-238.
44 Ha JH, Kim ML, Choi C, Choi IS, Myoung J, Ha SD. 2015. Recovery of structurally intact norovirus from food-contact surfaces. Food Control 47: 564-568.   DOI
45 Park SY, Kang SJ, Ha SD. 2016. Antimicrobial effects of vinegar against norovirus and Escherichia coli in the traditional Korean vinegared green laver (Enteromorpha intestinalis) salad during refrigerated storage. Int. J. Food Microbiol. 238: 208-214.   DOI
46 Ha JH, Choi C, Ha SD. 2014. Evaluation of immunomagnetic separation method for the recovery of hepatitis A virus and GI.1 and GII.4 norovirus strains seeded on oyster and mussel. Food Environ. Virol. 6: 290-296.   DOI
47 Lee JW, Cha DS, Hwang KT, Park HJ. 2003. Effect of $CO_2$ absorbent and high-pressure treatment on the shelf-life of packaged kimchi products. Int. J. Food Sci. Technol. 38: 519-524.   DOI
48 Jung JH, Lee KH, Puligundla P, Ko SH. 2013. Chitosanbased carbon dioxide indicator to communicate the onset of kimchi ripening. Lebensm. Wiss. Technol. 54: 101-106.   DOI
49 Lim JH, Park SS, Jeong JW, Park KJ, Seo KH, Sung JM. 2013. Quality characteristics of kimchi fermented with abalone or sea tangle extracts. J. Korean Soc. Food Sci. Nutr. 42: 450-456.   DOI
50 Bang YS, Joh YG, Moon SI. 1985. The change of free amino acid composition during radish kimchi fermentation. J. Korean Home Econ. Assoc. 23: 55-60.
51 John U, Hansen FK. 1976. Kinetics and mechanism of emulsion polymerization. Rubber Chem. Technol. 49: 536-609.   DOI
52 Lee NJ, Chun JK. 1981. Studies on the kimchi pasteurization. Part 1. Method of kimchi pasteurization with Chinese cabbage kimchi and its effect on the storage. J. Korean Agric. Chem. Soc. 24: 213-217.
53 Lee HA, Song YO, Jang MS, Han JS. 2013. Effect of Ecklonia cava on the quality kimchi during fermentation. J. Korean Soc. Food Sci. Nutr. 42: 83-88.   DOI
54 Jeong ST, Kim JG, Kang EJ. 1999. Quality characteristics of winter Chinese cabbage and changes of quality during the kimchi fermentation. Korean J. Postharvest Sci. Technol. 6: 178-183.