Research Communication
Behavior of Salmonella typhimurium DT104 during the manufacture and storage of pepperoni

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Abstract

Pepperoni batter (ca. 70% pork:30% beef) was prepared and subsequently inoculated with a six-strain cocktail (ca. 4.4×107 per gram batter) of Salmonella typhimurium DT104. After fermentation at 36°C and 92% relative humidity (RH) to ≤pH 4.8, counts of the pathogen decreased by about 1.3 log10 units. An additional 1.6 log10 unit decrease was observed following drying at 13°C and 65% RH to a moisture protein ratio (M/Pr) of 1.6:1. After storage of pepperoni sticks for 56 days under vacuum at 4 or 21°C, counts of the pathogen were about 4.6 and 6.6 log10 units lower, respectively, compared with starting levels in the batter. These data establish that fermentation and drying result in about a 3.0 log10 reduction in numbers of S typhimurium DT104 in pepperoni sticks and that storage of pepperoni sticks under vacuum at ambient temperature is more severe on the pathogen than refrigerated storage.

Introduction

Isolates of Salmonella typhimurium definitive phage type 104 (DT104) were first observed in 1984 in the United Kingdom (UK). Subsequently, the widespread and frequent association of DTlO4 isolates with farm animals or foods derived therefrom has been observed (Hollingsworth, 1997). Phage type 104 strains of Salmonella are resistant to multiple antibiotics, usually displaying resistance to ampicillin, chloramphenicol, streptomycin, sulfonamides, and tetracycline (R-type ACSSuT) (Threlfall et al., 1996). More recently, some strains have been isolated which also display resistance to trimethoprim and fluoroquinolones (Threlfall et al., 1996). In the UK, DT104 strains of S. typhimurium were second only to phage type 4 strains of S. enteritidis as the most prevalent Salmonella strains isolated (Threlfall et al., 1996). In the United States (US), S. typhimurium was also the second most commonly reported serotype of Salmonella (Hosek et al., 1997). Among S. typhimurium strains in the US, the DT104 phenotype was identified in 32% (90 of 282 isolates) of isolates tested during 1996, as compared to a prevalence of 28% (273 of 976 isolates) in 1995 and 7.0% in 1990 (Hosek et al., 1997).

Contact with ill farm animals and consumption of beef, chicken, pork sausage, and meat paste were identified as risk factors for DT104 infections in the UK (Davies et al., 1996, Wall et al., 1994). Although humans may have been the original source that subsequently spread this bacterium to animals (Anonymous, 1997), far less is known about the reservoir or risk factors for S. typhimurium in the US. A 1996 outbreak of salmonellosis among Nebraska elementary school children was attributed to S. typhimurium DT104 (Hosek et al., 1997). This US outbreak was linked to consumption of expired chocolate milk, but the organism was never cultured from the remaining cartons nor was the organism isolated from a kitten or turtle handled by children who became ill (Anonymous, 1997, Hosek et al., 1997).

In 1995, the United States Department of Agriculture (USDA) Food Safety and Inspection Service (FSIS) began requiring manufacturers of dry and semi-dry fermented sausage to validate processes to insure a 5-log10-unit reduction in numbers of Escherichia coli O157:H7 (Reed, 1995). In mid-1997, the USDA/FSIS indicated that when a plant could not demonstrate compliance with that requirement, more frequent sampling of products from the plant for E. coli O157:H7, as well as for Salmonella species and Listeria monocytogenes, would be required (Billy, 1997). Although information on the behavior of S. typhimurium in fermented meats was published some years ago (Goepfert and Chung, 1970, Masters et al., 1981, Smith et al., 1975),no information exists on the fate of S. typhimurium DT104 in fermented meats. However, there has been at least one report confirming the recovery of S.typhimurium DT104 from a stick of salami that displayed a plasmid profile identical to the plasmid profile from an isolate from a patient who consumed the same salami and became ill (Wall et al., 1994). There has also been at least two recalls of fermented meats due to Salmonella contamination, a recall of Lebanon bologna in 1995 (United States Department of Agriculture, 1995) and a recall of cervelat in 1997 (United States Department of Agriculture, 1997). The association of S. typhimurium DT104 with exposure to live animals and foods derived therefrom and the higher hospitalization and mortality rates for DT104 isolates compared with non-typhoid salmonellae, as well as the likelihood of more aggressive testing of fermented meats for Salmonella, prompted us to evaluate the viability of this bacterium after fermentation, drying, and storage of pepperoni.

Section snippets

Materials and methods

Six clinical isolates of Salmonella typhimurium were used. Those were: (i) strains H3380 and H3402 (phage type DT104); (ii) strains H3278 and H2662 (phage type DTlO4b); and (iii) strains G8430 and G7601 (phage type U302). All six isolates displayed an indistinguishable genomic fingerprint as determined by pulsed-field gel electrophoresis (data not shown). The salmonellae were maintained at −20°C in brain heart infusion (BHI; Difco Laboratories Inc., Detroit, MI) broth plus 10% glycerol and

Results and discussion

Previous studies have evaluated the fate of Salmonella in fermented meats. As one example, Smith et al. (1975)reported about a 1.3 log10 reduction in numbers of S. typhimurium after fermentation (35°C, 85% RH, pH 4.5) and about a 3.0 log10 reduction in pathogen numbers after drying (12°C, 65% RH, 22 days) of pepperoni. As other examples, Goepfert and Chung (1970)reported a 0.75 to 2.5 log10 reduction of S. typhimurium after fermentation (30°C, 90% RH, ≤pH 4.8) of Thuringer sausage and Masters

Acknowledgements

We extend our appreciation to Tim Lorang for invaluable suggestions and assistance, to Doskocil Food Service Company for providing meat, spices, and casings, and to Peggy Hayes and Bala Swaminathan of the CDC for providing isolates of S. typhimurium. This work was supported, in part, by contributions to the University of Wisconsin-Madison Food Research Institute from the Food Industry and, in part, by the College of Agricultural and Life Sciences of the University of Wisconsin-Madison.

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