Abstract

Campylobacteriosis is the most common cause of bacterial gastroenteritis worldwide. Consumption of chicken meat is considered the main route for human infection with Campylobacter. This study aimed to determine the critical factors for Campylobacter cross-contamination in Chinese commercial kitchens during chicken handling. Five commercial kitchens were visited to detect Campylobacter occurrence from 2019 to 2020. Chicken samples (n = 363) and cotton balls from the kitchen surfaces (n = 479) were collected, and total bacterial counts and Campylobacter spp. were detected. Genotypic characterization of 57 Campylobacter jejuni isolates was performed by multilocus sequence typing (MLST). In total, 77.41% of chicken carcass samples and 37.37% of kitchen surfaces showed Campylobacter spp. contamination. Before chicken preparation, Campylobacter spp. were already present in the kitchen environment; however, chicken handling significantly increased Campylobacter spp. prevalence (p < 0.05). After cleaning, boards, hands, and knives still showed high bacterial loads including Campylobacter spp., which related to poor sanitary conditions and ineffective handling practices. Poor sanitation conditions on kitchen surfaces offer greater opportunities for Campylobacter transmission. Molecular typing by MLST revealed that Campylobacter cross-contamination occurred during chicken preparation. The most prevalent sequence types, ST693 and ST45, showed strong biofilm formation ability. Consequently, sanitary condition of surfaces and biofilm formation ability of isolates were the critical points contributing to spread of Campylobacter in kitchen environment. These results provide insight into potential targeted control strategies along the farm-to-plate chain and highlight the necessity for improvements in sanitary conditions. The implementation of more effective cleaning measures should be considered to decrease the campylobacteriosis risk.

Highlights

  • Campylobacter is an important foodborne pathogen causing bacterial gastroenteritis worldwide [1]

  • During food preparation in domestic kitchens, there are two main transmission routes resulting in human ingestion: (i) the cross-contamination route, where Campylobacter avoid heating by transmission through taps, hands, and raw vegetables, and (ii) the heating route, where pathogens remain on the chicken meat but are only partly inactivated by heating [8]

  • A total of 479 samples were collected from sample sites, including the handler’s hands, knives, boards, containers, countertops, floors, and sinks, and of these, 179 samples tested positive for Campylobacter (37.37%)

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Summary

Introduction

Campylobacter is an important foodborne pathogen causing bacterial gastroenteritis worldwide [1]. 1 million individuals are infected by Campylobacter each year with an overall incidence of 16.5 cases per 10,000 in the United States [2,3], 64.8 cases per 10,000 in Europe [1], and 37.3–161.4 cases per 10,000 in China [4]. During food preparation in domestic kitchens, there are two main transmission routes resulting in human ingestion:. (i) the cross-contamination route, where Campylobacter avoid heating by transmission through taps, hands, and raw vegetables, and (ii) the heating route, where pathogens remain on the chicken meat but are only partly inactivated by heating [8]. A previous study identified the ability of foodborne pathogens to transmit from contaminated foods, such as chicken meat, to hands and direct contact surfaces in the domestic kitchen environment [11]. The cross-contamination and transfer rates for Campylobacter spp. have been well studied in domestic kitchens [12,13,14,15], the cross-contamination process is complicated and might be affected by many factors related to the characteristics of the bacteria, the contact surfaces, and processes employed [8]

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