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The Effect of Reuterin on <I>Listeria Monocytogenes</I> and <I

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The Effect of Reuterin on <I>Listeria Monocytogenes</I> and <I 1275 Journal of Food Protection, Vol. 61, No. 10, 1998, Pages 1275-1280 Copyright ©, International Association of Milk, Food and Environmental Sanitarians The Effect of Reuterin on Listeria monocytogenes and Escherichia coli 0157:H7 in Milk and Cottage Cheese M. G. EL-ZINEyl,2 AND J. M. DEBEVEREh lDepartment of Food Technology and Nutrition, Faculty of Agricultural and Applied Biological Sciences, University of Ghent, B-9000 Ghent, Belgium; and 2Department of Dairy Science and Technology, Alexandria University, Alexandria, Egypt MS 97-128: Received 17 July 1997/Accepted 2 February 1998 Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/10/1275/1670818/0362-028x-61_10_1275.pdf by guest on 26 September 2021 ABSTRACT A broad-spectrum reuterin produced during anaerobic fermentation of glycerol by Lactobacillus reuteri strain 12002 was found to be inhibitory and bactericidal for Listeria monocytogenes and Escherichia coli OI57:H7. Lyophilized reuterin was prepared by a two-step fermentation process. A batch fermentation in a IS-liter fermentor was applied to produce a maximum biomass of L. reuteri using a modified MRS broth at pH 4.3. Further, harvested cells were used to ferment glycerol (250 mM) under anaerobic conditions, The sensitivity to reuterin of 10strains of Listeria spp., including 6 strains ofL. monocytogenes, and 6 strains of E. coli, including one enterotoxigenic E. coli strain and two enterohemorrhagic E. coli strains, was estimated. Strains of L. monocytogenes were more resistant to reuterin than E. coli strains. In cottage cheese, pH 5.4, L. monocytogenes increased by 0.4 log while E. coli 0157:H7 decreased by 0.5 log in 21 days at 7°C; addition of reuterin (50 to 250 units per g) to the cottage cheese reduced the viability of both organisms. The inactivation rate was more pronounced (P :=; 0.05) with E. coli 0157:H7 than L. monocytogenes and it was dependent on reuterin concentration. The rate of E. coli 0157:H7 population reduction reached to 2, 3, and 6 log cycles by day 7 for reuterin concentrations of 50, 100, and 150 units per g of creamed cottage cheese, respectively. While, 100, 150, and 250 units of reuterin per g caused reductions in L. monocytogenes counts by 2, 5, and greater than 5 log cycles, respectively. In UHT skim milk with 150 units of reuterin per ml, stored at rc, the decline in the numbers of L. monocytogenes cells was higher than that in cottage cheese. Milk fat in the range of 0.5 to 3% did not affect the reuterin activity (P :=; 0.05). Addition of 3% salt enhanced the lethal effect of reuterin and diminished the initial population of L. monocytogenes by 4.5 log cycles in three days at 7°C. Reuterin is a potent broad-spectrum antimicrobial sub- tions of 50 and 100 units per g in ground beef kept at 4°C for stance produced by Lactobacillus reuteri during anaerobic 6 days reduced the viability of coliforms by 0.5 and 2 log fermentation of glycerol (3, 10). Reuterin exhibits an cycles respectively, while the viability increased by 4 log inhibitory activity against a wide range of microorganisms cycles in the control (8). including gram-positive and gram-negative bacteria, yeast, In recent years Listeria monocytogenes and Escherichia and fungi (5, 19). Reuterin has been isolated and identified coli 0157:H7 have become the most recognizable pathogens as an equilibrium mixture of monomeric, hydrated mono- of concern to public health and food agencies and the food meric, and cyclic dimeric forms of a metabolic intermediate, industry because of several outbreaks and cases associated l3-hydroxypropionaldehyde (29). with consumption of foods including milk and dairy prod- Reuterin is a neutral water-soluble product, effective in ucts (12, 21). It has been suggested that dairy cattle are a a wide range of pH (2 to 8) and resistant to proteolytic and natural reservoir for E, coli 0157:H7 (20). Further, it is lipolytic enzymes (5, 28). These advantages raise the known that L. monocytogenes can cause mastitis and possibility of applying reuterin successfully in a variety of abortion leading to excretion of the organism in milk from foodstuffs to increase their safety and extend their shelf life. the infected animal (15,16). Recently, L. reuteri has been applied to foods as a It has been reported that in cottage cheese L. monocyto- probiotic and/or starter culture. In bio-milk, named "BRA" genes survived fermentation and manufacturing processes in Sweden, the organism is used as an additional culture with (17, 25) whereas, E. coli 0157:H7 was able to multiply (1). Lactobacillus acidophilus and Bifidobacter spp. (26). It is also included in the production of Emmental-type cheese in Further, these organisms remained viable during storage at France (9). However, there is limited information concern- refrigeration temperatures (1, 17, 23, 25). Hence, the ing the application of reuterin in different food systems. In potential risk of consumption of milk or contaminated soft primary study, it is reported that reuterin added at concentra- cheese such as cottage cheese with L. monocytogenes or E. coli 0157:H7 prompted us to investigate the efficacy of reuterin in reducing the viability of these pathogens in * Author for correspondence. Mailing address: Department of Food Tech- cottage cheese at refrigeration temperature (70C) and to nology and Nutrition, University of Ghent, Coupure Links 653, B-9000 Ghent, Belgium. Tel: +32/92646177: Fax: +32/92255510; E-mail: johan. determine the effect of fat and salt content on reuterin [email protected]. activity in milk. 1276 EL-ZINEY AND DEBEVERE J. Food Prot., Vol. 61, No. 10 MATERIALS AND METHODS flow rate of 0.6 ml/min (10 mM H2S04 eluant); 20 111sample, loop injected, at 30°C. Reuterin was detected by refractive index Microorganisms. The strains of Listeria spp. included six measurement with a model RI 1047 detector (Hewlett-Packard). strains of L. monocytogenes, LMG 10470 (serotype I), LMG The retention time of reuterin under these conditions was 15 min; 13305 (serotype 4b), Ohio (OH, serotype 4b, isolated from reuterin eluted between glycerol (14 min) and trimethylene glycol Liederkranz cheese manufactured in Ohio), Scott A (clinical (18 min). Reuterin produced by the known producer strain DSM isolate, serotype 4b), V7 (milk isolate, serotype Ib, provided from 20016 (3) was used as a reference for reuterin. The presence of M. Bergdoll, The Food Research Institute, University of Wiscon- reuterin in the collected fractions was confirmed by the method of sin), and 121 (serotype 4b, associated with the outbreak of Circle et al. (6) and by the biological activity assay (5). listeriosis in Demark in 1989 and obtained from the Danish Research Meat Institute). Other Listeria strains used were Listeria Quantification of reuterin. Reuterin activity was quantified innocua strain LMG 11387, Listeria ivanovii strain LMG 11388, by the MIC method as described by Chung et al. (5). In general, the Listeria seeligeri strain LMG 11383, and Listeria welshimeri strain culture of E. coli LMG 8223 (indicator strain) grown overnight was LMG 11389. The strains of E. coli used through this study included harvested, washed twice with phosphate buffer (pH 7.2, 50 mM), Downloaded from http://meridian.allenpress.com/jfp/article-pdf/61/10/1275/1670818/0362-028x-61_10_1275.pdf by guest on 26 September 2021 verotoxigenic E. coli (VTEC) strain LMG 8223, Kl2 strains LMG suspended in the same buffer, and diluted to an A420 of 0.2 2579 and LMG 2578, enterotoxigenic E. coli (ETEC) strain CIP measured with a Shimadzu spectrophotometer (Shimadzu, Tokyo). 81.86 (Louis Pasteur Institute, Paris), and E. coli 0157:H7 strains This suspension was diluted III 0, which corresponds to about 6 932 (obtained from K. Glass, The Food Research Institute, 10glO CFU/ml. The diluted suspension (0.1 ml) was used to University of Wisconsin) and MRK 1542 (provided by Robert inoculate 1 ml of serial dilutions of reuterin diluted in basal Clark, University of Guelph, Ontario). Other strains woce from the medium (BM) containing (per liter in distilled water) 3 g casein Laboratory of Microbiology, University of Ghent, Belgium. L. hydrolysate, vitamin-free (Difco); 1.9 g ammonium citrate; 0.63 g monocytogenes strain OH and E. coli 0157:H7 strain 932 were citric acid; 12.6 g KH2P04; and 0.2 g MgS04·7H20; the pH was used in cottage cheese experiments. Survival experiments in the adjusted to 7.0 prior to autoclaving and 20 mM of filter-sterilized reuterin-treated UHT milk were performed using L. monocyto- glucose was added after sterilization. The tubes were incubated at genes OH. Cultures were maintained in tryptone soy broth (TSB, 3rC for 48 h. Growth was examined after 24 and 48 h. Reuterin Oxoid, Basingstoke, U.K.) containing 50% glycerol at -70°C and concentration was defined as the reciprocal of the highest dilution were propagated in TSB supplemented with 0.6% yeast extract that did not permit visible growth of the indicator strain. (TSYB) at 3rC. The cultures were transferred to individual tubes Determination of MIC values of reuterin against Listeria of the same broth and incubated at 3rC for 18 hprior to use. spp. and E. coli. The previously described method of Chung et al. Reuterin production. A reuterin producer strain L. reuteri (5) was followed with some modification. The MIC assay was strain 12002 was isolated from pig intestine and identified (11) performed in microtiter plates (Flow Laboratories, Rockville, Md.). using computerized comparisons of total soluble protein patterns Quantified reuterin was serially diluted in Mueller-Hinton medium (SDS-PAGE) as described by Pot et al. (24). Concentrated reuterin (Difco) supplemented with 20 mM glucose. The tested strains were used in the milk and cheese experiments was prepared by a grown in TSYB for two successive cultures at 3rC for 24 h.
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