Broiler Campylobacter contamination and human campylobacteriosis in Iceland

Abstract

To examine whether there is a relationship between the degree of Campylobacter contamination observed in product lots of retail Icelandic broiler chicken carcasses and the incidence of human disease, 1,617 isolates from 327 individual product lots were genetically matched (using the flaA short variable region [SVR[) to 289 isolates from cases of human campylobacteriosis whose onset was within approximately 2 weeks from the date of processing. When there was genetic identity between broiler isolates and human isolates within the appropriate time frame, a retail product lot was classified as implicated in human disease. According to the results of this analysis, there were multiple clusters of human disease linked to the same process lot or lots. Implicated and nonimplicated retail product lots were compared for four lot descriptors: lot size, prevalence, mean contamination, and maximum contamination (as characterized by direct rinse plating). For retail product distributed fresh, Mann-Whitney U tests showed that implicated product lots had significantly (P = 0.0055) higher mean contamination than nonimplicated lots. The corresponding median values were 3.56 log CFU/carcass for implicated lots and 2.72 log CFU/carcass for nonimplicated lots. For frozen retail product, implicated lots were significantly (P = 0.0281) larger than nonimplicated lots. When the time frame was removed, retail product lots containing Campylobacter flaA SVR genotypes also seen in human disease had significantly higher mean and maximum contamination numbers than lots containing no genotypes seen in human disease for both fresh and frozen product. Our results suggest that cases of broiler-borne campylobacteriosis may occur in clusters and that the differences in mean contamination levels may provide a basis for regulatory action that is more specific than a presence-absence standard.

FIG. 1.

Unrooted maximum likelihood tree of Campylobacter flaA SVR alleles. Alleles present in human isolates are marked with a filled circle. Alleles present in broiler samples are marked with an open square. Numbers above branches indicate bootstrap support (out of 1,000 bootstrap replicates) for the nodes. The bar along the bottom indicates branch length as substitutions per site.

FIG. 2.

Frequency distribution of time between onset of symptoms and receipt of the fecal sample in the reference laboratory for cases of human campylobacteriosis.

FIG. 3.

Comparison of fresh-product lots implicated in human disease to those not implicated in human disease. Black bars show the numbers of implicated lots. Gray bars show the numbers of nonimplicated lots. (A) Lot size. (B) Prevalence. (C) Mean contamination. (D) Maximum contamination.

FIG. 4.

Comparison of frozen product lots implicated in human disease to those not implicated in human disease. Black bars show the numbers of implicated lots. Gray bars show the numbers of nonimplicated lots. (A) Lot size. (B) Prevalence. (C) Mean contamination. (D) Maximum contamination.

FIG. 5.

Comparison of fresh-product lots containing Campylobacter flaA SVR alleles also seen in human disease (“WITH”) to lots containing no alleles seen in human disease (“WITHOUT”). Black bars show the numbers of “WITH” lots. Gray bars show the numbers of “WITHOUT” lots. (A) Lot size. (B) Prevalence. (C) Mean contamination. (D) Maximum contamination.

FIG. 6.

Comparison of frozen product lots containing Campylobacter flaA SVR alleles also seen in human disease (“WITH”) to lots containing no alleles seen in human disease (“WITHOUT”). Black bars show the numbers of “WITH” lots. Gray bars show the numbers of “WITHOUT” lots. (A) Lot size. (B) Prevalence. (C) Mean contamination. (D) Maximum contamination.