Journal of Food Protection, Vol. 55, No. 2, Pages 98-103 (February 1992) Copyright©, International Association of Milk, Food and Environmental Sanitarians

Use of acidilactici to Control Listeria monocytogenes in Temperature-Abused Vacuum-Packaged Wieners

ALAN J. DEGNAN, AHMED E. YOUSEF1, and JOHN B. LUCHANSKY* Downloaded from http://meridian.allenpress.com/jfp/article-pdf/55/2/98/1662953/0362-028x-55_2_98.pdf by guest on 02 October 2021 Food Research Institute, Department of and Toxicology, University of Wisconsin-Madison, 1925 Willow Drive, Madison, Wisconsin 53706

(Received for publication August 5, 1991)

ABSTRACT slaughter house (9,13) and processing environment (5,14), and handling of meats during and/or after processing con­ JBL1095 (pediocin AcH producer) tributes to the prevalence of the pathogen in meat products and P. acidilactici LB42 (bacteriocin nonproducer) were evalu­ (9,29,30). The incidence of L. monocytogenes ranges from ated for the production of antilisterial compounds in packages of 0 to 92% in fresh meats, and from 3 to 13% in ready-to-eat all-beef wieners. Commercially processed, freshly manufactured, unpackaged wieners were surface inoculated (ca. 105 CFU/g) as products (6,18,30). The high incidence of the pathogen on follows: (i) untreated control; (ii) a three-strain (Scott A, V7, meats does not necessarily correlate with elevated counts of 101M) mixture of Listeria monocytogenes; (iii) strain JBL1095; L. monocytogenes in positive samples. Typical counts of (iv) L. monocytogenes and strain JBL1095; and (v) L. monocyto­ the pathogen range from <10 to 1000 CFU/g in raw and genes and strain LB42. Wieners were vacuum packaged and cell processed products (3,14). However, counts of >104 CFU/ numbers, pH, and bacteriocin activity within packages were deter­ g were recovered in pate (20), and counts of 103-106 CFU/ mined following storage at refrigeration (4°C) or abuse (25°C) g were recovered from contaminated prepacked sliced meats temperatures for 72 and 8 d, respectively. L. monocytogenes and (28). Other studies revealed that the pathogen can survive, pediococci survived in packages held at 4°C, but pediococci did and in some instances grow, in ready-to-eat meat products not produce acid or pediocin during refrigerated storage. At 25°C, total numbers of L. monocytogenes (treatment ii) increased 3.2 such as ham, wieners, bologna, and bratwurst (12), as well as sliced frankfurter-type sausages (26) and wiener exu­ log10 CFU/g and the pH of the fluid (exudate) within packages increased from 5.5 to 5.6. In contrast, L. monocytogenes survived dates (32). but did not grow in packages inoculated with strain LB42 (treat­ Although thermal processing is an effective method to ment v), and was inhibited (average reduction of 2.7 log 0 CFU/ eliminate undesirable , including Listeria (33), the g) in packages inoculated with strain JBL1095 (treatment iv) presence of L. monocytogenes in meats at the retail level during storage at 25°C for 8 d. The pH of exudate in packages suggests that problems with this pathogen arise largely as a inoculated with strains JBL1095 (treatment iv) or LB42 (treatment consequence of postprocessing contamination (9,14,15,29, v) showed a similar decline (ca. 5.5 to 4.6). The onset of bacteriocin production coincided with early-logarithmic growth of 30). Additional, perhaps novel, control measures are needed JBL1095 (treatment iv) and continued into the late logarithmic to minimize the potential for microbial hazard. "Natural" phase. These data suggest that bacteriocinogenic pediococci can methods of controlling undesirable bacteria, including L. be used to control L. monocytogenes in temperature-abused, cook/ monocytogenes, in meats (15) may be appealing to "food chili meats. additive-conscious" consumers. Natural preservatives such as organic acids, peroxides, and/or bacteriocins produced by pediococci have potential for use as biocontrol agents. Listeria monocytogenes is a facultative intracellular Pediococci have already found extensive use as starter pathogen responsible for several foodborne disease out­ cultures in meat fermentations, and some strains have been breaks (8). Although red meats have not been involved in used experimentally for controlling L. monocytogenes in outbreaks of listeriosis, sporadic illness has been linked to minced meat (16,25), fermented sausage (1,24), raw meat pate (20), and an epidemiologic association of listeric (21), and wiener exudate (32). In this study, we expand illness and ingestion of non-reheated wieners has been efforts to employ biopreservation systems and compare the established (27). L. monocytogenes is prevalent in both the efficacy of a bacteriocinogenic to a nonbacteriocinogenic strain of pediococci for controlling the growth of L. mono­ cytogenes in packaged wieners stored at abuse (25°C) and 'Department of Food Science & Technology, 122 Vivian Hall, 2121 Fyfferefrigeratio n (4°C) temperatures. Rd„ Ohio State University, Columbus, OH 43210-1097.

JOURNAL OF FOOD PROTECTION, VOL. 55, FEBRURAY 1992 CONTROL OF LISTERIA IN WIENERS 99

MATERIALS AND METHODS incubated at 25°C. A single package from each treatment incu­ bated at 4°C was sampled at 14-d intervals for up to 72 d. For Bacterial strains packages incubated at 25°C, one package of each treatment was Table 1 lists bacteria used in this study. Pediococci were sampled daily for 8 consecutive d. Two trials of this experiment maintained as frozen (-20°C) stocks in TGE (2) broth plus 10% were made. glycerol, and passed twice (at 37°C for 24 h) in TGE broth before use. L. monocytogenes strains were maintained and cultured as pH monitoring described previously (32). One corner of the sampled package was cut to prepare a sampling port of sufficient size to insert a 10-ml pipet or pH TABLE 1. Designations, characteristics, and origins of bacteria electrode. Values for pH of wiener exudate (fluid naturally present used.' inside the package) were determined by inserting a sanitized and calibrated electrode (Corning Scientific Products, Corning, NY) Strain Relevant characteristics Origin or reference directly into the package.

P. acidilactici Enumeration of bacteria Exudate was aseptically removed from packages via the JBL1095 Bacr Bac+ (pSMB74) (32) sampling port using a 10-ml pipet. The volume removed was Downloaded from http://meridian.allenpress.com/jfp/article-pdf/55/2/98/1662953/0362-028x-55_2_98.pdf by guest on 02 October 2021 strdO riM measured and released back into the package, and then the total JBL1146 LB42 Bacs Bac (plasmid free) Ray2 volume of fluid in the package was adjusted to 20 ml with sterile 1 % NaCl solution. After folding and clamping the package at the L. monocytogenes sampling port, each package was hand massaged (40 to 60 s) to dislodge bacteria adhering to wieners or package linings. For JBL1000 Scott A Clinical isolate, serotype 4b Marth3 enumeration of L. monocytogenes, the exudate-saline solution was JBL1002 101M Meat isolate, serotype 4b (11) removed from wiener packages and 0.1-ml portions, or dilutions JBL1004 V7 Raw milk isolate, serogroup 1 Marth3 thereof, were surface plated onto McBride's Listeria agar (17) containing 5 g lithium chloride per L. Plates were incubated for 48 'Abbreviations: Bac+, bacteriocin producer; Bac', bacteriocin re­ h at 37°C, and colonies that were ca. 2 mm diameter and weakly sistant; Bac, non-bacteriocin producer; str-10, streptomycin resis­ beta-hemolytic were counted and confirmed as L. monocytogenes tant (1000 jug/ml); rif-1. rifamycin resistant (100 jug/ml). (23). P. acidilactici JBL1095 (StrrRif mutant of P. acidilactici H) 2B. Ray, Department of Animal Science, University of Wyoming, was enumerated by surface plating appropriate dilutions of the Laramie, WY. exudate-saline solution onto MRS (Difco) agar containing 1000 3E. H. Marth, Department of Food Science, University of Wiscon­ |ig Str and 100 |ig Rif per ml (32). Colonies of JBL1095 were sin, Madison, WI. counted following incubation at 37°C for 48 h. P. acidilactici LB42, the predominant (LAB) in treatment v, Inocula preparation was enumerated on MRS agar plates. Using this method, as few 2 A three-strain mixture of L. monocytogenes (101M, V7, and as 0.5 CFU/g of wieners (1 x 10 CFU per package) could be Scott A) used as a "cocktail" was prepared as follows: cells (20 detected. ml) of 24-h old cultures of each strain were sedimented by centrifugation (7600 x g, 5 min, 4°C), and the resulting pellets Bacteriocin activity were resuspended in a nominal volume of 1% peptone (Difco The "spot-on-lawn" method (22) was used to assay for Laboratories Inc., Detroit, MI) water. Individual cell suspensions antilisterial activity. Bacteriocin activity was expressed as arbi­ (ca. equal concentrations) were combined, and the final volume trary units (AU) per 5 |il supernatant as the inverse of the highest was adjusted to 10 ml with peptone water. This cell mixture was dilution showing a definite zone of clearing using L. monocyto­ diluted in peptone water to a final concentration of about 107 genes 101M, V7, or Scott A as indicators. To verify that antilisterial CFU/ml. Cell suspensions of strains JBL1095 and LB42 of activity in wiener packages was caused by a bacteriocin, exudate- Pediococcus acidilactici were prepared separately as described saline solution from packages inoculated with JBL1095 were earlier for L. monocytogenes, and the final volume was adjusted incubated with proteinase K (4.9 units/ml; Sigma Chemical Co., to yield about 107 pediococci per ml. St. Louis, MO). Loss of antilisterial activity in proteinase-treated exudate indicated the presence of pediocin AcH. Treatment preparation Freshly processed, unpackaged, all-beef wieners (ca. 40 g/ Statistical analysis link) were obtained from a commercial processor. Wieners were D values for L. monocytogenes were calculated from the held at 5°C, then treated and packaged within a few hours of their slope (b) of the line fitted to data (log CFU/g vs d of storage) by manufacture. Wieners were placed (5 per package) in 10 x 7.5 in. linear regression (D-value = -1/b). Growth data were analyzed by heat-sealable nylon bags (permeability = <3 ml 02 and 1 ml H,0 the logistic model (7,10) as employed previously (31). Model per 100 in2 per 24 h at 73°F and 0% relative humidity; Curwood, parameters were used to estimate the lag period, generation time, New London, WI). The following treatments were prepared: (i) and maximum growth of bacteria in some experiments. uninoculated control, (ii) L. monocytogenes only, (iii) P. acidilac­ tici JBL1095 only, (iv) P. acidilactici JBL1095 plus L. monocy­ RESULTS togenes, and (v) P. acidilactici LB42 plus L. monocytogenes. Cell suspensions (0.2 ml) of bacteria were randomly distributed drop- Recovery of bacteria from packages wise to the surface of wieners throughout a package using a 1-ml A preliminary experiment was conducted to evaluate pipette. Packages were hand massaged and then heat sealed under our ability to recover bacteria inoculated into wiener pack­ vacuum (-14.9 psi) using a Multivac Vacuum Packer (Koch ages. Packages were inoculated with 7.0 x 10s and 4.0 x 105 Manufacturing, Kansas City, MO). Sixteen packages were pre­ pared for each treatment; one set of eight packages for each CFU of P. acidilactici JBL1095 or L. monocytogenes, treatment was incubated at 4°C, and the remaining set was respectively, and then vacuum sealed. Packages were incu-

JOURNAL OF FOOD PROTECTION, VOL. 55, FEBRUARY 1992 100 DEGNAN, YOUSEF AND LUCHANSKY bated at 25°C for 1 h, and then samples of the exudate - Both P. acidilactici JBL1095 and LB42 grew in wiener saline solution were removed and plated. Recovery was packages, and estimated growth parameters are shown in 91% (6.4 x 105 CFU) for P. acidilactici JBL1095 and 85% Table 2. These data revealed that strains LB42 and JBL1095 (3.4 x 105 CFU) of L. monocytogenes. did not differ appreciably in their growth patterns within Yousef et al. (32) used MRS agar to enumerate lactic wiener packages, and that the presence of L. monocyto­ acid bacteria (LAB) associated with all-beef wieners. In genes had no apparent effect on the growth of strain this study, packages inoculated with P. acidilactici JBL1095 JBL1095. (treatments iii or iv) gave similar counts on selective (MRS agar plus Str and Rif) and nonselective (MRS agar) media. These data revealed that JBL1095 was the predominant 6.0 - LAB in inoculated packages and, therefore, counts on MRS agar were also used to estimate total numbers of P. /^ acidilactici LB42 (treatment v). 5.0 -ft-- -8 o __*/

Indigenous flora and pH values of uninoculated packages Downloaded from http://meridian.allenpress.com/jfp/article-pdf/55/2/98/1662953/0362-028x-55_2_98.pdf by guest on 02 October 2021 E3 \ O A Numbers of LAB in uninoculated packages (treatment \ • 4.0 - \ i) held at 4°C were initially below the limits of detection. \ However, after 72 d counts increased to a maximum of 4.8 - \ o •\ \ log CFU/g. Similarly, freshly packaged wieners did not o - \ \ contain sufficient exudate to allow the initial pH to be _J3.0 - \ • \• x • measured. The pH of exudate monitored within uninoculated - \ packages stored at 4°C decreased from 5.7 (day 1) to 5.0 \ - \ S3 2.0 - (day 72). At 25°C, total numbers of indigenous LAB in \ uninoculated packages (treatment i) increased (0.6 to 5.98 log CFU/g) and the pH decreased from 5.6 to 5.1 between - 1.0 ' > i i 1 ' • days 1 and 8, respectively. 123456789 DAYS Behavior of listeriae and pediococci in packages held at 4°C Figure 1. Behavior of L. monocytogenes in the presence of Total numbers of L. monocytogenes or P. acidilactici pediococci in wiener packages stored at 25°C for 8 d (trial 2). in packages of all-beef wieners did not change significantly Symbols represent data points, linear sections represent data during storage at 4°C for up to 72 d. Counts of L. mono­ fitted by linear regression, and the curved line represents the cytogenes decreased 0.46 log CFU/g, whereas numbers of growth curve fitted by the logistic model. (0--0), strain mixture strain JBL1095 decreased approximately 0.54 log 0 CFU/g. (Scott A, V7, and 101M) of L. monocytogenes; (U-O), the strain Likewise, the pH of exudate did not change appreciably mixture of L. monocytogenes in the presence of P. acidilactici over the 72-d sampling period, and pediocin AcH activity JBL1095; (A-A), the strain mixture ofL. monocytogenes in the was not recovered from packages stored at 4°C. It seems presence of P. acidilactici LB42. likely that insufficient growth precluded acid and bacterio- cin production by JBL1095 incubated at 4°C in packages of wieners. . _B fl_ _ • - _-'^, ---*- — z — s - / 4 Control of L. monocytogenes in wiener packages held at 8.0 - / / • - 25°C J 1 ,'a/ /" \7.0 - The behavior of listeriae (alone and in combination ! i b€ with pediococci) inoculated into wiener packages was moni­ • i , ; 1 / U tored during storage at 25°C for 8 d (data for one trial are 6.0 / 1 / o y i f shown in Fig. 1). Growth or death parameters (estimated o 1 statistically) for bacteria included in these experiments are / n/ I 1 - _ D/ / shown in Table 2, and data presented in this section are

averages (two trials) of these estimates. L. monocytogenes 4.0 - (treatment ii) in wiener packages held at 25°C had a lag

• period of 4.1 d and a generation time of 0.33 d (7.8 h), and III , , I 1 1 3.0 -A- / Ill numbers of the pathogen increased 3.2 log CFU/g during 4 5 6 the storage period. In contrast, counts of L. monocytogenes DAYS decreased slightly (0.33 log CFU/g) in packages contain­ 10 Figure 2. Behavior of pediococci and activity of bacteriocin in the ing strain LB42 and decreased appreciably (2.7 log CFU/g) presence of L. monocytogenes in packaged wieners during stor­ in the presence of JBL1095. age at 25°C for 8 d. (trial 2). Symbols represent data points and curved lines represent growth curves as predicted by the logistic Activities of pediococci in wiener packages held at 25°C model. (U-U) P. acidilactici JBL1095; (A-A), P. acidilactici Changes in bacterial growth, pH, and bactericidal ac­ LB42; (<>—<>), activity (Arbitrary Units/g of wieners) of pediocin tivity were monitored within wiener packages held at 25°C. AcH in wiener packages containing P. acidilactici JBL1095.

JOURNAL OF FOOD PROTECTION, VOL. 55, FEBRURAY 1992 CONTROL OF LISTERIA IN WIENERS 101 TABLE 2. Parameters for growth or inactivation of L. monocy­ togenes and P. acidilactici in wiener packages held at 25°C for 8 d.

Strains Treat- Trial Growth parameters D value enumerated ment Laga G.T.b Max. G.c (d)

L. monocytogenes ii 1 3.0 0.30 8.1 — 2 5.2 0.35 5.9 - L. monocytogenes iv 1 - - - 3.5 ffi 2 - - - 2.5 P< d L. monocytogenes V 1 - - - ND 2 — - - 24

P. acidilactici JBL1095 iii 1 0.40 0.098 8.6 — 2 0.79 0.14 8.5 — Downloaded from http://meridian.allenpress.com/jfp/article-pdf/55/2/98/1662953/0362-028x-55_2_98.pdf by guest on 02 October 2021 P. acidilactici JBL1095 iv 1 0.50 0.10 8.5 — 2 0.79 0.15 8.5 — P. acidilactici 4 5 6 LB42 V 1 ND ND ND — DAYS 2 1.1 0.14 8.4 - Fieri 3. pH values (trial 2) of exudates from packages of aLag period (d). wieners inoculated with pediococci andlor listeriae and stored at feneration time (d). 25°Cfor 8 d. (O-O), strain mixture (Scott A, V7 and 101M) of

'Maximum growth (log]0 CFU/g wieners). L. monocytogenes: (Q--Q), P. acidilactici JBLJ095 and the strain dND = not determined. mixture of L. monocytogenes; (A--A), P. acidilactici LB42 and the strain mixture of L. monocytogenes.

Although the populations of both LB42 and JBL1095 intimates that innovative approaches should be explored to increased steadily during storage at 25°C for 8 d, bacteri­ control the pathogen should improper processing, or subse­ cidal activity was detected only from packages inoculated quent contamination, or temperature abuse occur. Alternate with JBL1095 (Fig. 2). Moreover, pediocin activity coin­ control measures proposed or in practice to preclude micro­ cided with the onset of logarithmic growth of JBL1095 and bial hazard include the use of nontraditional additives (e.g., remained relatively constant throughout the stationary phase liquid smoke, sodium lactate), postprocessing pasteuriza­ of growth. Inhibition due to hydrogen peroxide was dis­ tion, product reformulation (e.g., reduced pH, aj, and/or counted because such inhibition was not detected in spot- reduced temperature storage. Recent studies revealed the on-lawn assays using unheated, cell-free supernatants from utility of biopreservation systems of LAB origin for con­ strain LB42 (treatment v). Furthermore, listericidal activity trolling L. monocytogenes in raw meats (21), fermented was not detected in treatment iii (P. acidilactici JBL1095 semidry sausage (7), minced meat (16), and salami and only) after treatment of exudate with proteinase K. fresh Mettwurst (25). Yousef et al. (32) demonstrated the efficacy of pediococci and pediocins for controlling L. Experiments were also performed to monitor pH monocytogenes associated with wieners. In this study, natu­ changes in packages of wieners inoculated with listeriae ral preservatives (i.e., organic acid and pediocin) were (treatment ii) and listeriae and pediococci (treatments vi evaluated for their antilisterial activity in packages of all- and v). The pH increased slightly (from 5.5 to 5.6) in beef wieners. packages inoculated with L. monocytogenes only (treatment L. monocytogenes survives and in some instances grows ii) during storage at 25°C. In packages inoculated with L. at refrigeration temperatures in processed meats [i.e., ham, monocytogenes and either JBL1095 or strain LB42, the pH bologna, and bratwurst (12), sliced frankfurter-type prod­ declined steadily and at equivalent rates from about 5.5 to ucts (28), and vacuum-packaged frankfurters (4)]. We about 4.6 over 8 d. These data (compare Fig. 1, 2, and 3) showed previously (32) that wiener exudates are listericidal indicated that listericidal activity within packages was asso­ and that L. monocytogenes does not grow in exudates ciated with the presence of P. acidilactici JBL1095 and the stored at 4°C for up to 29 d. We report herein that L. production of pediocin AcH by this strain. monocytogenes does not grow in vacuum-sealed packages DISCUSSION of wieners stored at 4°C for 72 d. In contrast, Buncic et al. (4) reported about a 3-log increase in numbers of L. Listeria monocytogenes is widely distributed in the monocytogenes in vacuum-packaged frankfurters during 20 environment and frequently isolated from fresh and ready- d of storage at 4°C. Differences in experimental approach to-eat meats, but listeric illness is not commonly associated may account, at least in part, for differences between our with eating red meats. The frequent association and sur­ results and the results of other investigators. More specifi­ vival/growth of L. monocytogenes in cooked, refrigerated cally, loss or depletion of wiener exudate during inocula­ meats portends the potential for microbial hazard, and tion or repackaging and/or differences in the type and

JOURNAL OF FOOD PROTECTION, VOL. 55, FEBRUARY 1992 102 DEGNAN, YOUSEF AND LUCHANSKY degree of smoking may explain the observed variations produced acid and pediocin AcH and displayed listericidal regarding the intrinsic antilisterial activity of vacuum-pack­ activity toward the pathogen (average D value = 3.0 d). aged wieners. Since strains LB42 and JBL1095 are phenotypically indis­ At a temperature (25°C) simulating product abuse, the tinguishable except for bacteriocin production/immunity, presence of P. acidilactici LB42 (treatment v) suppressed the data presented herein argue strongly that production of growth of the pathogen but did not result in a decrease in pediocin AcH by JBL1095 potentiated the antilisterial ac­ total numbers of L. monocytogenes. Factors other than pH tivity of lactic acid bacteria in vacuum-packaged wieners. may also have contributed to the listeriostatic effect of These studies confirmed that biocontrol systems could strain LB42 against L. monocytogenes (e.g., P. acidilactici provide an additional hurdle for listeriae to circumvent in LB42 may have depleted nutrients required for growth of L. certain cook/chill meats. Future efforts are directed to monocytogenes). The listeriostatic effect resulting from incorporate biocontrol systems during product formulation addition of P. acidilactici LB42 to wiener packages com­ for more facile and homogenous applications to a variety of pared favorably with previous investigations evaluating the foods. antilisterial activity of LAB. For example, L. monocyto­ ACKNOWLEDGMENTS genes grew in sausage batter fermented without added Downloaded from http://meridian.allenpress.com/jfp/article-pdf/55/2/98/1662953/0362-028x-55_2_98.pdf by guest on 02 October 2021 starter culture, but growth of the pathogen was not detected We extend our appreciation to Michael P. Doyle for many insightful when LAB were used to ferment the batter (11,24). In discussions, and to Bibek Ray for providing P. acidilactici LB42. contrast to results obtained with strain LB42, the presence This project was supported in part by the Beef Industry Council of off. acidilactici JBL1095 in wiener packages resulted in the National Livestock and Meat Board, the College of Agriculture and death of the pathogen due to the production of pediocin Life Sciences, University of Wisconsin-Madison, and by contributions to the Food Research Institute. AcH. Significant listericidal activity was detected in exu­ dates after the onset of the logarithmic phase of growth of REFERENCES P. acidilactici JBL1095 in packages stored at 25°C. Similar to results obtained with wiener exudates (32), the produc­ 1. Berry, E. D., M. B. Liewen, R. W. Mandigo, and R. W. Hutkins. tion of pediocin AcH by P. acidilactici JBL1095 reduced 1990. Inhibition of Listeria monocytogenes by bacteriocin-producing the population of L. monocytogenes in wiener packages Pediococcus during the manufacture of fermented semidry sausage. J. Food Prot. 53:194-197. compared to otherwise similar packages that did not con­ 2. Biswas, S. R„ P. Ray, M. C. Johnson, and B. Ray. 1991. Influence tain pediococci or pediocin. of growth conditions on the production of a bacteriocin, pediocin Food is a complex media in which various compo­ AcH, by Pediococcus acidilactici H. Appl. Environ. Microbiol. nents, alone or in combination, affect bacterial growth. In 57:1265-1267. 3. Buchanan, R. L., H. G. Stahl, M. M. Bencivengo, and F. del Corral. the environment within packages of wieners, components 1989. Comparison of lithium chloride-phenylethanol-moxalactam such as nitrates, NaCl, phenols, and organic acids (4,12,19) and Modified Vogel Johnson agars for detection of Listeria spp. in contribute toward suppressing microbial growth; however, retail-level meats, poultry, and seafood. Appl. Environ. Microbiol. it is difficult to directly correlate this effect to any single 55:599-603. 4. Buncic, S., L. Paunovic, and D. Radisic. 1991. The fate of Listeria component (32). Natural preservation systems such as monocytogenes in fermented sausages and in vacuum-packaged frank­ bacteriocinogenic LAB and/or associated bacteriocins may furters. J. Food Prot. 54:413-417. find utility for controlling the occurrence and dissemination 5. Doyle, M. P. 1988. Effect of environmental and processing condi­ of L. monocytogenes in meats. In this regard, numbers of L. tions on Listeria monocytogenes. Food Technol. 42(4): 169-171. 6. Farber, J. M., F. Tittiger, and L. Gour. 1988. Surveillance of raw- monocytogenes were reduced approximately 1 and 2 log fermented (dry cured) sausages for the presence Listeria spp. Can. CFU/g of minced meats (25) and sausage (7), respectively, Inst. Food Sci. Technol. J. 21:430-434. in the presence of LAB biocontrol systems. As reported 7. Garrett, M. K., S. T. C. Weatherup, and M. D. B. Allen. 1978. Algal herein, however, P. acidilactici JBL1095 was listericidal culture in the liquid phase of animal slurry. Effect of light and temperature upon growth and phosphorus removal. Environ. Pollut. towards L. monocytogenes in vacuum-packaged wieners. 15:141-154. The reduction in pH by JBL1095 was not solely respon­ 8. Gellin, B. G., and C. V. Broome. 1989. Listeriosis. J. Am. Med. sible for the death of Listeria: the pH of exudates in Assoc. 261:1313-1320. packages containing P. acidilactici JBL1095 was similar to 9. Genigeorgis, C. A., D. Dutulescu, and J. F. Garayzabal. 1989. Prevalence of Listeria spp. in poultry meat at the supermarket and that in packages containing strain LB42, and strain LB42 slaughterhouse level. J. Food Prot. 52:618-624. did not exhibit listericidal activity. Moreover, the 2.7-log 10. Gibson, A. M., N. Bratchell, and T. A. Roberts. 1987. The effect of reduction (Fig. 1) in counts of L. monocytogenes by JBL1095 sodium chloride and temperature on the rate and extent of growth of in packages held at 25°C is significant, because the number Clostridium botulinum type A in pasteurized pork slurry. J. Appl. Bacterid. 62:479-490. of listeriae contaminating retail-level sliced frankfurter- 11. Glass, K. A., and M. P. Doyle. 1989. 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