Prevalence, antibiotic resistance and genotypes of Campylobacter jejuni and Campylobacter coli isolated from chickens in Irbid governorate, Jordan
Introduction
Campylobacteriosis is a disease caused by members of Campylobacter sp. In low and middle income countries (LMICs) infection in toddlers is mainly caused by C. jejuni (Oberhelman and Taylor, 2000), although C. coli, C. fetus and C. upsaliensis can also infect humans. Ingestion of only 500 cells may cause acute diarrhea to humans (Whiley et al., 2013).
All poultry species can carry Campylobacter; however, chickens pose a greater risk to humans due to the frequency of consumption (Humphrey et al., 2007). Consumption of raw or undercooked chicken or cross-contaminated from raw chicken can result in clinical cases (Nadeau et al., 2002). There is always a potential risk of contamination of chicken meat with Campylobacter, if hygienic measures are not applied properly during processing (Osaili et al., 2012). In Jordan, butcher shops (informal, small-scale chicken-slaughterhouses that sell directly to consumers) are still operating, which is the case in many other LMICs. These informal slaughtering facilities are characterized by poor hygiene, inadequate facilities, lack of cold, clean water and inspection during processing. As a result, they are likely to pose a higher risk for consumers (Carron et al., 2017; Cook et al., 2017). Data on Campylobacter infection in poultry in Jordan are available. A study carried out in 2012 found Campylobacter jejuni in around 40% of the studied broiler farms (Osaili et al., 2012). Al-Natour et al. (2018) investigate the occurrence of Campylobacter in 35-layer farms in Northern Jordan and found C. jejuni in 40% of chicken cloacae. More recently, a longitudinal study on a single semi-commercial poultry farm, suggests that there may be differences in the transmission dynamics of Campylobacter in this type of farms (which are an important source of poultry for the Jordanian population) and those observed in poultry farms in high-income countries, with potentially an earlier introduction of the pathogen into the flock, but slower within-flock transmission (Neves et al., 2019). Data on the presence of Campylobacter in poultry products in Jordan are limited, but evidence from other countries strongly suggests that Campylobacter is likely to be present in retail poultry in Jordan. A review conducted in 2009 suggests that in most countries, in which studies have been conducted, a majority of poultry products on retail are contaminated with Campylobacter (Suzuki and Yamamoto, 2009). According to the European Food Safety Agency (EFSA) in 2011, in Europe 8 out of 10 chickens were contaminated with Campylobacter sp. (EFSA, 2011). The frequency of Campylobacter in frozen samples is not common and freezing is suggested as a way for decontaminating slaughtered birds (Ilida and Faridah, 2012),
Macrolides, such as erythromycin and azithromycin, are the treatment of choice for Campylobacter, alternatively, fluoroquinolones (ciprofloxacin) and tetracycline can also be used (Osaili and Alaboudi, 2017; Siddiqui et al., 2015a, Siddiqui et al., 2015b). In severe cases such as bacteremia, aminoglycosides (gentamicin) are also used (Alfredson and Korolik, 2007; Corcoran et al., 2006; Kurinčič et al., 2007). Nevertheless, Campylobacter resistant strains have increased, probably as a result of the increased use and misuse of antibiotics in poultry farms (Silva et al., 2011), with strains being particularly resistant to chloramphenicol, tetracycline, macrolides, and fluoroquinolones (Cody et al., 2010; EFSA, 2011; Silva et al., 2011).
Currently, Multilocus Sequence Typing (MLST) is the leading and most discriminative method for genotyping (Duarte et al., 2016). It implies the use of housekeeping genes (6–7 genes), which may represent the genome for MLST (Dingle et al., 2001). Relying on the fact that the proteins, which encode these housekeeping genes, evolve slowly, MLST will provide data for accurate phylogenic estimation, typing and strain relatedness (Maiden, 2006). Therefore, the aims of the study were to determine i) the occurrence of C. jejuni and C. coli in chickens at informal butcher shops (fresh), formal poultry slaughterhouses (refrigerated) and retail market (frozen) and ii) the antimicrobial resistance, genotypes and relatedness of the isolates.
Section snippets
Sample collection
The following formula (Krousel-Wood et al., 2006) was used to determine sample size:
n = (1.96)2PQ/d2, whereas:
n = sample size required.
1.96 z value at α-error = 0.05
P = prevalence of the disease.
Q = 1 – P.
d = tolerated margin of error.
The reported prevalence rate from previous local studies for chickens was 34.4%, Accordingly the number of samples was determined as:
n = ((1.96)2 × 0.344 X (1–0.344))/(0.07)2
n = 177.
Over the period January to May 2017, 177 fresh, refrigerated (not more than
Occurrence of Campylobacter in chicken
Out of 177 chicken samples 64 samples (36.2%), had morphology compatible with that of Campylobacter reference strains. Biochemical tests identified C. coli in 40 samples and C. jejuni in 18. Final confirmation of the isolates was carried out using PCR. The results confirmed that 36 of the isolates were C. coli and the remaining 20 isolates were C. jejuni. The frequency of Campylobacter spp. among the studied samples of local chicken from butcher shops (fresh), local chicken from formal
Discussion
Chicken meat has been identified as the main source of human Campylobacter infection and studies aiming at attributing the source of human infection or the relatedness of isolates are conducted (Nadeau et al., 2002; Ravel et al., 2017). The occurrence of Campylobacter among chickens sold in Jordan included in this study (31.6% overall among fresh, refrigerated and frozen) is comparable to results from different countries such as Italy 34% (Stella et al., 2017), China 45% (Zhu et al., 2017),
Acknowledgment
This work was part of the OIE Veterinary Education Twinning Programme between The Royal Veterinary College and the Jordan University of Science and Technology funded by the World Organization for Animal Health (OIE) and partly funded by Deanship of research at Jordan University Science and Technology (grant number 365/2017).
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