An overview of Campylobacter infection in the turkey industry

Alessandra PICCIRILLO - Department of Comparative Biomedicine and Food Science, University of Padua, Legnaro (PD), Italy

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Thermophilic Campylobacter spp. are bacteria causing a human disease called campylobacteriosis, which is characterized by gastrointestinal symptoms such as fever, acute diarrhoea and abdominal cramps. In rare cases (1 in 1000), Campylobacter spp. (mostly C. jejuni) are associated with severe autoimmune-mediated demyelinating neuropathies, such as Guillain-Barrè and Miller-Fisher syndromes.

Antimicrobial therapy is required for severe, complicated and systemic forms of the disease. Fluoroquinolones (e.g. ciprofloxacin) and macrolides (e.g. erythromycin) are the drugs of choice. Among thermophilic Campylobacter spp., C. jejuni is the species most commonly involved in human infections (90% of cases), followed by C. coli (6%), C. upsaliensis, and C. lari.

Thermophilic Campylobacter spp. are ubiquitous in the environment, where they can survive for long periods. Campylobacter are also harboured in the alimentary tract of a variety of wild and domesticated birds and mammals, mainly food-producing animals. Among these, poultry represent the main reservoir, harbouring Campylobacter at high concentrations, but rarely showing clinical signs. Research studies have demonstrated that Campylobacter are widespread in the poultry production systems, including meat turkeys. The handling and the consumption of contaminated raw or undercooked poultry meat are considered the major sources of human infection.

Despite the large consumption of turkey meat worldwide, most research on thermophilic Campylobacter spp. in poultry has focused on broiler production and few studies have been carried out on meat turkeys. In Europe, few Member States (MS) report surveillance data on turkeys and turkey products. In 2013, 3 MS reported prevalence data ranging from 0% to 100% (average 33,96%) of Campylobacter-positive turkeys and 12 MS reported data ranging from 0% to 50% (average 14,56%) of Campylobacter-positive turkey meat (at slaughter, processing and retail) (EFSA & ECDC, 2015).

Campylobacter contamination may occur at all stages of the turkey production chain. The high prevalence of Campylobacter in the primary production represents a risk for contaminating the poultry carcasses during processing. Differences in Campylobacter prevalence rates may depend on several factors, such as geographical area, time period, husbandry conditions, production practices, biosecurity measures, climate, antimicrobial treatment regimens, slaughter techniques, hygienic standards during processing. Studies carried out at pre-harvest level have shown that turkeys can be colonized by either C. jejuni and C. coli.

The exclusive presence of C. jejuni or C. coli and the concurrent presence of both species in the same flock have been reported. An alternating predominance of one Campylobacter spp. over the other and transient peaks in C. jejuni and C. coli loads over time have also been observed. Thanks to advanced molecular typing tools (i.e. PFGE, flaSVR typing, and MLST), a wide variety of Campylobacter genotypes has been detected in turkey flocks. Some flocks may be infected with only one genotype, while others with more than one genotype. Different strains in individual flocks may be replaced or displaced by others during the same rearing cycle.

The onset of Campylobacter colonization in turkeys is variable and several reasons have been pointed out to explain the difference (e.g. maternal antibodies, antibiotic feed additives, intestinal development and intestinal microbial flora). Newly hatched poults are usually free of infection and, although Campylobacter have been isolated from all segments of the female reproductive tract, vertical transmission has not been demonstrated yet. Initial colonization of turkeys, therefore, occurs mainly through horizontal transmission and has been reported as early as within 7 days from the hatch and as late as by 18 weeks of the rearing cycle. Once a flock has been colonized, a very rapid bird-to-bird spread of Campylobacter determines the colonization of the entire flock within a few days, thanks to the efficient fecal-oral transmission route. Self-limitation of the infection has been rarely documented and a flock usually remains colonized at high levels until slaughter, resulting in carcass contamination during processing.

About the sources for Campylobacter transmission in turkey flocks, very little is known. Many potential vehicles, such as contaminated drinking water, insects (e.g. flies, lesser mealworms, etc.), wild birds, other animals on the farm (e.g. dogs, rodents, cattle and sheep), farm personnel and equipment have been pointed out, but it is still difficult to define the most likely source of flock colonization, since not always same strains from birds are also isolated from environmental sources. The effect of season on the occurrence of Campylobacter colonization has been reported, with higher positivity rates during the summer months compared to the winter months.

Studies carried out at post-harvest level have shown that, as for live animals, turkey meat (several parts of the carcass and fresh, chilled or frozen meat) can be contaminated with both Campylobacter spp. (C. jejuni and C. coli) with a relative prevalence of the two species, even though many studies report a predominance of C. jejuni versus C. coli. By using genetic typing methods it has also been shown that a wide variety of genotypes can be found on turkey meat. Some genotypes in turkey flocks can be recovered from carcasses throughout the entire processing line up to the final product. During processing, Campylobacter-negative flocks can be contaminated by the same genotypes introduced into the slaughterhouse by positive flocks. On the other hand, some genotypes can be found in the carcasses only after some stages of the processing (e.g. air chilling) suggesting other sources, other than Campylobacter-positive flocks, for carcass contamination inside the processing plant.

Cross-contamination of carcasses can originate from live birds colonized during the rearing period and from other sources in the processing plant.

Usually, Campylobacter contamination of carcasses derives from the introduction of Campylobacter-positive turkey flocks into the slaughter plant.Although a reduction of Campylobacter contamination occurs, they can persist on the carcass after processing. Therefore, a single Campylobacter-positive flock may represent a contamination risk for Campylobacter-negative flocks. 

Among the risk factors increasing the potential of Campylobacter carcass contamination, the transportation of turkeys from the farm to the slaughterhouse and the slaughter process logistics are those most commonly involved. Studies have suggested that transport-induced stress can increase the intestinal bacterial load and the fecal Campylobacter isolation rates after transport. Other studies have found that the high temperature of the defeathering water (54-56 °C), the rupture of intestines during the evisceration, and the drying of the carcass skin during air chilling (24 h at 2 °C) are critical stages of the slaughter process for carcass contamination. As for live animals, seasonality in Campylobacter contamination rate has been detected in turkey meat, with a higher prevalence during the summer than during the winter.

In the last years, an increase in antimicrobial resistance and multidrug-resistance has been documented in thermophilic Campylobacter spp. both from turkeys and turkey meats. Resistance has been commonly detected against fluoroquinolones, macrolides, and tetracyclines, and more rarely to other classes of antimicrobials (e.g. sulphonamides, aminoglycosides, etc.). Generally, resistance to certain antimicrobials is significantly higher in C. coli than in C. jejuni. Furthermore, several studies have shown that some of these resistances are typically transferable. Therefore, antimicrobial resistance of turkey Campylobacter may pose serious concern both for animal and human health, since antimicrobial resistant strains can be transmitted to humans through the food chain.

Currently, no effective prevention and control strategies to reduce the prevalence of thermophilic Campylobacter spp. in turkey production seem to exist. Control of Campylobacter should be first realized at the primary production level and then in the food chain. A detailed understanding of the epidemiology of Campylobacter in turkeys is strongly needed, since only when the sources for Campylobacter transmission will be individuated, intervention strategies would be implemented.

(From Proceedings of the 9th Turkey Science and Production Conference, Chester, UK)