Phenotypic and molecular typing of Salmonella strains reveals different contamination sources in two commercial pig slaughterhouses

Abstract

This study aimed to define the origin of Salmonella contamination on swine carcasses and the distribution of Salmonella serotypes in two commercial slaughterhouses during normal activity. Salmonellae were isolated from carcasses, from colons and mesenteric lymph nodes of individual pigs, and from the slaughterhouse environment. All strains were serotyped; Salmonella enterica serotype Typhimurium and Salmonella enterica serotype Derby isolates were additionally typed beyond the serotype level by pulsed-field gel electrophoresis (PFGE) and antibiotic resistance profiling (ARP); and a subset of 31 serotype Typhimurium strains were additionally phage typed. PFGE and ARP had the same discriminative possibility. Phage typing in combination with PFGE could give extra information for some strains. In one slaughterhouse, 21% of the carcasses were contaminated, reflecting a correlation with the delivery of infected pigs. Carcass contamination did not result only from infection of the corresponding pig; only 25% of the positive carcasses were contaminated with the same serotype or genotype found in the corresponding feces or mesenteric lymph nodes. In the other slaughterhouse, 70% of the carcasses were contaminated, and only in 4% was the same genotype or serotype detected as in the feces of the corresponding pigs. The other positive carcasses in both slaughterhouses were contaminated by genotypes present in the feces or lymph nodes of pigs slaughtered earlier that day or from dispersed sources in the environment. In slaughterhouses, complex contamination cycles may be present, resulting in the isolation of many different genotypes circulating in the environment due to the supply of positive animals and in the contamination of carcasses, probably through aerosols.

FIG. 1.

Dendrogram based on combination of the PFGE patterns of Salmonella serotype Derby isolates after XbaI and SpeI DNA digestion. The main PFGE types are numbered; subtypes are designated by lowercase letters. Arrows indicate small differences within a genotype.

FIG. 2.

Dendrogram based on combination of the PFGE patterns of a selection of Salmonella serotype Typhimurium isolates after XbaI and BlnI DNA digestion. The main PFGE-types are numbered; subtypes are designated by lowercase letters. Arrows indicates small differences within a genotype.

FIG. 3.

Correlation in time among Salmonella-positive carcasses (▵) and Salmonella positivity of feces (○) or of feces and/or mesenteric lymph nodes (•) of incoming animals in slaughterhouse A2 (left) and slaughterhouse D1 (right).

FIG. 4.

Distribution of Salmonella types at each time point when 250 pigs passed the slaughter line in slaughterhouse A2. (A) Positive samples from feces and/or mesenteric lymph nodes of pigs; (B) positive carcasses. Numbers in bars represent serotypes and genotypes as follows: 1, serotype Brandenburg; 2, serotype Typhimurium T11/T11; 2′, serotype Typhimurium T11/T11a; 3, serotype Derby D1; 4, serotype Derby D2a; 5, serotype Derby D2b; 6, serotype Derby D3; 7, serotype Derby D4; 8, serotype Infantis; 9, serotype Typhimurium T9; 10, serotype Virchow; 11, serotype Livingstone; 12, serotype Typhimurium T8/T8; 12′, serotype Typhimurium T8/T12; 13, serotype Typhimurium T4/T4; 13′, serotype Typhimurium T4/T4a; 14, serotype Typhimurium T5; 15, serotype Ohio O1; 16, serotype London; 17, serotype Typhimurium T3; 18, serotype Typhimurium T6; 19, serotype Rissen; 20, serotype Typhimurium T1; 21, serotype Goldcoast.

FIG. 5.

Distribution of Salmonella types at each time point when 350 pigs passed the slaughter line in slaughterhouse D1. (A) Positive samples from feces and/or mesenteric lymph nodes of pigs; (B) positive carcasses. Numbers in bars represent serotypes and genotypes as follows: 1, serotype Typhimurium T8/T8 (AChSuST); 2, serotype Typhimurium T10 (ChSuT); 3, serotype Typhimurium T8/T8 (AChSuT); 4, serotype Typhimurium T_ND (ChSuST); 5, serotype Typhimurium T2/T2 (susceptible); 5′, serotype Typhimurium T2a/T2a (ChSu); 6, serotype Infantis; 7, serotype Anatum; 8, serotype Havana; 9, serotype Derby D2a (SuT); 10, serotype Agona; 11, serotype Derby D1b (AChSuTNal); 12, serotype 47:Z4213:-; 13, serotype Panama; 14, serotype Derby D1 (A); 15, serotype Livingstone.

FIG. 6.

Number of isolates for every genotype or serotype recovered from pig samples (feces and mesenteric lymph nodes) (open bars), carcasses (shaded bars), and the environment (solid bars) for slaughterhouses A2 (A) and D1 (B).