10.4.1.1 Meat Products

In a screening exercise involving 221 strains of Lactobacillus species evaluated for their ability to

inhibit the growth of microorganisms commonly occurring in meat products [87], a wide range of

bacteria were found to be affected by individual strains: e.g., Serratia marcescens (by 47% of the

strains), Citrobacter freundii (47%), Proteus vulgaris (67%), S. typhimurium (9%), and Brochothrix

thermosphacta (87%). In most cases, the inhibitory activity of the protective culture was attributed to

lactic acid formation, although 6 of the 221 LAB isolates (all isolates of Lactobacillus sake) formed a

bacteriocin contributing to the inhibition of L. monocytogenes. Experiments performed by the same

researchers on comminuted cured pork (German-type fresh Mettwurst) with pH 5.7 were aimed at control

of L. monocytogenes and showed that a strain of Lactobacillus sake producing a suitable antilisterial

bacteriocin was able to reduce the growth potential of the pathogen by about 1 log cycle [86]. A

mutant of Lactobacillus sake that did not produce the bacteriocin did not affect the number of Listeria

inoculated into this product. In another study using Lactobacillus sake as the protective culture, the

control of L. monocytogenes in vacuum-packaged sliced Brühwurst (cooked sausages) was emphasized

[65]. Sliced sausage samples were inoculated with a mixture of four L. monocytogenes serovars,

fortified with either one of two bacteriocin-producing strains of Lactobacillus sake, isolate Lb706,

which produced sakacin A, and isolate Lb674, which produced sakacin 674, or of a nonbacteriocinproducing

strain of Lactobacillus sake and stored for up to 28 days at 7°C. While the nonbacteriocinproducing

LAB reduced counts of L. monocytogenes but not to an acceptable extent, both

bacteriocin-producing strains of Lactobacillus sake were able to control growth of L. monocytogenes

adequately at the high initial counts tested.

Using bacteriocin-producing and nonbacteriocin-producing strains of Pediococcus acidilactici for protection

of turkey summer sausages against L. monocytogenes, Luchansky [67] found that the pathogen

could be reduced by the bacteriocin producer by 3.4 log cycles, but only by 0.9 log cycle when the nonbacteriocin-

producing strain was used. In vacuum-packaged wiener and frankfurter sausages, proliferation

of L. monocytogenes inoculated in the products was suppressed for over 60 days by addition of

P. acidilactici JD1-23 at 107 CFU/g product, whereas the viable count of the pathogen increased from 104

to 106 in the control [12]. Degnan et al. [29] observed a clear antilisterial effect of yet another bacteriocinproducing

strain of P. acidilactici in vacuum-packaged wieners stored at abuse temperature (25°C), where

the addition of the protective culture resulted in a reduction of L. monocytogenes counts by 2.7 log cycles

within 8 days while pathogen counts increased by 3.2 log cycles in sausages without added pediococci. In

bacon, a pediocin-producing strain of P. acidilactici has been used in combination with reduced levels of

nitrite to prevent toxin production due to the outgrowth of C. botulinum spores. Here, the protective culture

would grow during conditions of temperature abuse, producing lactic acid and inhibitory pediocins.

Strain P. acidilactici H, isolated from fermented sausage, exhibited a broader range of bactericidal activity

than any other pediococcal bacteriocin due to the production of a bacteriocin termed pediocin AcH.

Pediocin producers have also been used as protective cultures relying on their lactic acid production,

rather than on the production of a bacteriocin. Hutton et al. [57] used the “Wisconsin process” (a combination

of lactic acid starter culture and sucrose) to prevent toxigenesis by C. botulinum in reduced

nitrite bacon. In chicken salads, these authors found that a combination of P. acidilactici and glucose prevented

botulinum toxigenesis. When the chicken salad was temperature abused, the protective culture

catabolized available glucose to lactic acid, which caused a decrease in the pH of the product. Pathogen

challenge tests verified that the rate and extent of lactic acid accumulation in the chicken salad

during temperature abuse was sufficient to preclude botulinum toxigenesis.

Kotzekidou and Bloukas [64] studied the effect of protective cultures on the shelf life of sliced

vacuum-packed cooked ham. They found that cooked ham produced with Lactobacillus alimentarius and

Staphylococcus xylosus as protective cultures was acceptable up to 28 days, while control ham had a

246 Handbook of Food Preservation, Second Edition

shelf life of 21 days. The activity of the protective cultures was directed toward micrococci, staphylococci,

and B. thermosphacta. Meat salads with relatively high pH values (pH 6.0–6.5) were studied by

Hennlich and Cerny [54] for potential application of LAB as protective cultures in limiting the hygienic

risks caused by food salmonellae, staphylococci, or clostridiae. The risk of pathogen growth in these

foods is most apparent under temperature-abuse conditions, and the research showed that distinct

cultures of LAB are indeed able to decrease microbial risks due to foodborne pathogens at elevated

temperature. While they do not reduce spoilage by bacilli, yeasts, or fungi, the protective cultures used

could reduce the growth of pathogens and actually spoiled the food before the pathogens could grow to

hazardous levels.

Andersen [3] recently reported on a commercial protective culture (“FloraCarn L2”) developed for

fresh sausages, which can be used as an additional safety and quality factor where contamination during

or after processing is a possible hazard. FloraCarn L2 was tested in fresh British sausage mince and was

shown to suppress the indigenous microflora and B. thermosphacta. In fresh coarse chopped sausages,

the protective culture inhibited the possible development of indigenous coliform bacteria during storage.

Research on protective cultures has not always found potential positive applications for bacteriocinproducing

LAB. Targeting at the control of L. monocytogenes in meats during long-term storage, Buncic

et al. [19] tested Lactobacillus sake 265 (Lb 265) and Lactobacillus casei 52 (Lb 52) isolated from

chilled meat products as protective cultures. Although both starter cultures produced bacteriocin at

4°C, they were not able to suppress growth of L. monocytogenes inoculated at 103 CFU/g on vacuumpackaged,

raw beef (pH 5.3–5.4) during 23 days’ storage at 4°C when they were inoculated at the same

low level. The protective cultures were equally ineffective when applied on vacuum-packaged emulsiontype

sausages (pH 6.4) inoculated with L. monocytogenes and stored at 4°C for 23 days. Apparently,

the amounts of bacteriocin produced in situ by the low initial numbers of protective cultures employed

were not sufficient to inhibit or reduce L. monocytogenes on chilled meats to any significant extent, and

higher initial numbers of LAB are not desirable in chilled meats for product quality reasons.

10.4.1.2 Fish and Seafood

Wessels and Huss [111] studied the use of protective cultures as inhibitors of L. monocytogenes in lightly

preserved fish products. Coculture of the pathogen with a nisin-producing strain of Lactococcus lactis

subsp. lactis at 30°C resulted in a decline of the pathogen from 5 _ 105 to _5 CFU/mL within 31 h.

However, when the protective culture was inoculated on slices of commercial cold smoked salmon stored

at 10°C for 21 days, no net growth was detected. Despite this lack of evidence of in situ proliferation of

the protective culture on cold smoked salmon slices coinoculated with L. monocytogenes (104 CFU/g)

and the protective culture (3 _ 106 CFU/g), the population of the pathogen declined by a half log cycle

during the first 15 days, then increased at a rate slightly lower than that of the control not inoculated with

the lactococcus. Although a complete reduction of the pathogen was not achieved, the experiments

proved the point that control of proliferation was feasible under practical conditions.

The use of bacteriocins from LAB for the preservation of brined shrimps, which are usually protected

from microbial deterioration by addition of sorbic or benzoic acid, was tested by Einarsson and Lauzon

[36]. Three different bacteriocins were evaluated (nisin Z, carnocin U149, and bavaricin A) for their

biopreservative potency. With nisin Z, the most effective bacteriocin, a delay in bacterial growth was

observed that resulted in an extension of the shelf life by 21 days (from 10 to 31 days). The strongest

preservative effect was found with sodium benzoate and potassium sorbate, which completely inhibited

microbial growth for 59 days when added to the brined shrimps at levels of 0.05%–0.1% (w/w).

In a recent overview paper, Huss et al. [56] presented an update on biopreservation used with fish

products as they discussed a range of relevant topics: biopreservation as a full or partial alternative to salt

or chemical additives, protective cultures and their characteristics, selection of protective cultures, and

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