Pathogenic Bacteria

Pork has been described as a source of human salmonellosis and, indeed, pigs are important carriers of Salmonella (11,12). Salmonella strains disseminate and multiply during slaughtering and cutting and are commonly found on pork carcasses and cuts (13,14). Salmonella have been shown to survive in naturally fermented pepperoni and Lebanon Bologna (15,16). Addition of starter cultures during manufacture of pepperoni and Lebanon Bologna decreases the viability of Salmonella. Rapid pH drop to below 5.3 proved to be important for inhibiting Salmonella when products are fermented at temperatures above 18°C (17). Growing conditions of Salmonella are a minimal pH of 5.0 and a minimal water activity (aw) of 0.95 (18). Thus, inhibition of Salmonella is mainly obtained by acidification by lactic acid bacteria in the norther technology and by drying in the southern one.

Staphylococcus aureus can be widely disseminated in meat because it is endemic in the processing environment (19). A study of pig hindquarters showed that 22.7% of the samples were contaminated by S. aureus, and counts from 103 to 106 cfu/cm2 were obtained in 10% of the positive samples (20). One or more staphylococcal enterotoxin genes were identified by PCR in 17% of samples of raw pork, salted meat, and ready-for-sale uncooked smoked ham (21). In the United States, the growth of S. aureus and the presence of enterotoxins in fermented sausages, particularly in Genoa and Italian-type dry salami, have caused various outbreaks of food poisoning (22). Growth of S. aureus is inhibited at pH 5.1 and aw 0.86 in aerobiosis, and at pH 5.7 and aw 0.91 in anaerobiosis (18). In the norther technology, the large diameter favors anaerobiosis and pH drops very quickly below 5.0; these conditions will inhibit the growth of S. aureus. In the southern technology, the small diameter of the sausages favors aerobiosis, pH is often superior to 5.1, and aw of 0.84-0.88 is only reached at the end of the drying period. None of the strains of lactic acid bacteria active in sausage fermentation has been found to efficiently inhibit S. aureus by means of bacteriocins (5). S. aureus constitutes a risk to health only after growth in a food product to levels of about 105 or 107 cells (5). Production of toxins is limited at aw 0.87 for toxin type A, 0.90 for type B, and 0.94 for type C (18). Thus, drying in the southern technology in which aw varies from 0.90 to 0.93 after fermentation (10) does not inhibit all toxin production by S. aureus.

Listeria monocytogenes is more frequently involved in sporadic cases of food poisoning. It is ubiquitous and can establish in plants as an in-house bacterium (23-25). It has been reported that as many as 68% of environmental samples in a curing plant were positive and 17% remained positive after cleaning (26). Recent European investigations have reported 12-16% Listeria-positive samples in fermented industrial products (27,28). There is no epidemiological evidence for the involvement of fermented sausages in recent outbreaks of listeriosis, and the International Commission on Microbiological Specification for Foods recommends that up to 100 cells of L. monocytogenes per gram of fermented meat products be tolerated (27,28). However, L. monocytogenes is slowly inhibited during sausage fermentation, and it is desirable to eliminate this microorganism from raw ready-to-eat meat products. L. monocytogenes can grow at pH levels between 4.6 and 9.6 and cannot grow below aw 0.90 (28). This means that drying during ripening limits its growth. Using lactic acid bacteria that produce bacteriocins active against L. monocytogenes can reduce the level of this pathogen in fermented sausages by about one or two log cycles compared to non-bacteriocin-producing bacteria with similar souring activity (5). This applies to various types of fermented sausages (Table 3). However, no reduction higher than two logs was noticed, which can be explained by interactions between bacteriocins and meat or fat materials (29).

Cattle are the main reservoir of enterohemorrhagic Escherichia coli (EHEC) but pigs are also implicated (30-32). Foods commonly associated with infection are of animal origin and include raw minced meat and fermented meats (33,34). The consumption of contaminated salami slices was responsible for an episode of food poisoning in 1994 in the United States. Indeed, E. coli O157:H7 has been reported to survive during manufacturing of sausages (35,36) and during storage of slices (37,38). Lactic acid bacteria can accelerate the destruction of EHEC by lowering the pH and thus facilitating drying.

B. Toxic Compounds: Biogenic Amines

Biogenic amines such as histamine, tyramine, cadaverine, and putrescine are low-molecular-weight compounds that are produced from amino acids by microbial decarboxylation. Some

Table 3 Effect of Various Bacteriocinogenic Lactic Acid Bacteria on Listeria in Fermented Sausages

Type of sausage

Bacteriocinogenic strains

Decimal reduction of Listeria counta

Fresh (low acid) Dried German type Spanish type

Italian type US type

L. sakei Lb706

L. sakei and L. curvatus strains L. sakei and L. curvatus strains Enterococcus faecium L. plantarum MCS P. acidilactici

No reduction

Slight effect on survival

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