From farm to fork follow-up of thermotolerant campylobacters throughout the broiler production chain and in human cases in a Hungarian county during a ten-months period

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Abstract

A study tracking thermotolerant campylobacters from the setting of the broilers throughout the whole rearing period, slaughter and sale of chicken products in five consecutive broiler rotations of the same henhouse as well as in two different other farms was conducted in a well-defined geographic area (Hajdú-Bihar county, Hungary) between March 2006 and Feb 2007. All notified cases of human campylobacteriosis in this area during the study period were also included. One hundred and one, 44, 23 and 282 Campylobacter jejuni and 13, 15, 20 and 60 C. coli were isolated from broiler houses, slaughterhouses, retail shops and human samples, respectively. Sixty-two isolates collected from broilers or their environment selected from different flocks (57 C. jejuni, 5 C. coli), 92 isolates collected from abattoirs and retail shops (72 C. jejuni, 20 C. coli), as well as 85 randomly selected human isolates (74 C. jejuni, 11 C. coli) were subjected to PFGE analysis using restriction enzymes KpnI and SmaI.

Sixty-six of the isolates produced unique Sma-Kpn profiles; the majority (46) of these were of human origin. The remaining isolates formed PFGE clusters of between 2–25 isolates with 14 (12 C. jejuni and 2 C. coli) main clusters comprised of five or more isolates with identical KpnI-SmaI patterns.

Two genetic clones of C. jejuni (clone A, n = 25; clone B, n = 20) included 18% of isolates from different sources. Generally, isolates from one cluster were found in 1–3 different flocks, notably, clone B was present in three rotations including those from the two independent farms. Six of the seven investigated flocks had one or two characteristic prevalent clones. Transmission of clones between consecutive flocks was frequently seen. Spread of both C. jejuni and C. coli was traced multiple times along the food chain; eight C. jejuni, but no C. coli clones were detected both in broilers and humans.

These data suggest that broilers were the major source for C. jejuni but not for C. coli in the studied area and period. For C. jejuni the carryover of strains between consecutive flocks may be a common event, but the strain is eventually replaced by another and consecutive carryover events seem to be infrequent. The majority of the human disease was due to nonepidemic strains; some clones were transmitted from more than one broiler flocks (including epidemiologically unrelated flocks) to humans multiple times.

Highlights

► We tracked thermotolerant Campylobacter spp. from farm to fork using PFGE. ► All studied flocks were positive at the flock and at the abattoir level. ► Multiple probable transmission events of C. jejuni was detected. ► Some C. jejuni genotypes were followed from farm to retail and to human infections. ► C. coli was less important in human disease in the study setting.

Introduction

Gastrointestinal infection with thermotolerant campylobacters cause significant morbidity both in developing and developed countries. The two most frequent species, Campylobacter jejuni and C. coli, are among the most frequent causes of bacterial enteritis in the European Union and in the United States (Humphrey et al., 2007, Moore et al., 2005). The caused disease burden is comparable to that of salmonellosis, and markedly exceeds those of other bacteria causing enteritis (European food safety authority, 2010b). In Hungary, the estimated number of cases of campylobacteriosis is 6000–10000 cases annually, corresponding to an incidence of 57.7 per 100000 inhabitants vs. a median morbidity of 47.1 per 100000 persons in the EU in 2007 (European food safety authority, 2010b). Besides gastroenteritis, severe sequelae may also occur (Humphrey et al., 2007). Most notified Campylobacter infections in Hungary are considered as sporadic and the sources of infection as well as possible related cases remain undiscovered in most cases.

Poultry has been recognized as the primary reservoir of C. jejuni and a significant reservoir of C. coli (Friedman et al., 2004, Humphrey et al., 2007, Sheppard et al., 2009). Epidemiological evidence points to the major role of zoonotic transmission of these pathogens from poultry to humans (Hakkinen et al., 2009, Moore et al., 2005, Sheppard et al., 2009). Recent studies suggest that some genotypes or clonal lineages adapted to animal host may never or only rarely cause disease in humans, whereas others are common human pathogens with one or several potential food-borne sources (Duim et al., 2003, Lindmark et al., 2004, Ragimbeau et al., 2008). A number of studies followed these bacteria between different points of the food chain (e.g. Hakkinen et al., 2009, Lienau et al., 2007, Lindmark et al., 2004, Parisi et al., 2007, Thakur et al., 2010, Zorman et al., 2006). Most of these studies investigate animal to food or food to human transmission, but reports encompassing the whole food chain from farm to fork are scant.

The aim of our study was to follow thermotolerant Campylobacter spp. throughout the whole food chain from farm to fork, i.e. from the broiler premises through the abattoir and the retail shops to human cases occurring in the region where the majority of the broiler meat from the studied stocks was sold.

Section snippets

Sample collection: broiler farms

During the study period (April 2006 – January 2007) five consecutively set and reared flocks (K1-K5, 15000 birds/flock) of a commercial broiler chicken farm (K) located in an eastern county of Hungary were visited and sampled regularly. At the end of the study period one broiler flock each from two other farms (farms N and D, 21000 and 15000 birds/flock, respectively) located in other municipalities of the same county were also included. The farms K and N belonged to the same owner (Owner 1),

Campylobacter prevalence

During the study period 398 C. jejuni and 121 C. coli isolates were recovered as follows: 101 C. jejuni and 13 C. coli from the seven broiler flocks in the three farms (K1-K5, D and N flocks); 72 C. jejuni and 29 C. coli from abattoir environment and meat samples; 23 C. jejuni and 19 C. coli from retail meat (Table 1); 202 C. jejuni and 60 C. coli from human faecal samples (out of 8044 stool samples examined).

Environmental, air, feed, water samples collected at setting as well as meconium samples and

Discussion

Transmission along the food chain (from broilers through the abattoir to the retail shop) is generally accepted as a major source of human campylobacteriosis (European food safety authority, 2010b, Hakkinen et al., 2009, Lienau et al., 2007, Lindmark et al., 2004, Parisi et al., 2007, Thakur et al., 2010, Zorman et al., 2006). However, epidemiological tracking of Campylobacter spp. is burdened by many problems (European food safety authority, 2010b), including, among others, simultaneous

Acknowledgements

The study was supported by a GVOP 3.1.1-2004-0472/3.0 grant.

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