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Simple Summary: Extended-spectrum cephalosporin (ESC)-resistant Enterobacteriaceae frequently detected in humans and food-producing animals are of major concern in public health. This study was undertaken to investigate the contamination of ESC-resistant E. coli in the environment of a slaughterhouse during chicken meat processing. This study indicates that cross-contamination of ESBL/AmpC-producing E. coli has a crucial impact on the occurrence of ESC resistance in retail chicken meat. Thus, ESBL-/AmpC-producing E. coli were brought into the slaughterhouse by certain broiler chicken flocks, and other chicken flocks were contaminated by ESBL/AmpC-producing E. coli already present in the slaughterhouse environment. These findings support the hypothesis that world widely epidemic conjugative plasmids have contributed to the dissemination of ESBL/AmpC resistance in broiler chickens in Korea. As conjugative plasmids always carrying multiple resistance genes, continuous persistence of blaCTX-M and blaCMY genes located on plasmids within microbial communities will be mediated by co-selection processes with other resistance genes. Hence, further research on the control of bacterial conjugation is urgently required. Our study emphasizes that chicken slaughterhouses could perform the functions of convergence and dispersion of ESBL/AmpC resistance, and that world widely epidemic conjugative plasmids contribute to the dissemination of ESBL/AmpC from chickens to humans along the food chain. ESC-resistant E. coli isolates were collected from broiler chickens, a slaughterhouse, and retail meat to assess their dispersion and their involvement in cross-contamination. ESBL-/AmpC-producing E. coli were isolated during the slaughter process of all six investigated chicken flocks from scalding, feather removal, first conveyor, evisceration, second washing, third conveyor, and third washing areas, and from handling workers in the slaughterhouse. ESC-resistant E. coli isolates with the same pulsed-field gel electrophoresis type were found in the same site (scalding) on different sampling days. ESBL/AmpC-producing E. coli isolates were absent in the lairage area in the slaughterhouse, but present in the retail markets in 36.8% (7/19) of the chicken flocks. The blaCTX-M genes and blaCMY-2 were conjugated to recipient E. coli J53 in 67.5% (27/40) and 56.1% (23/41) of ESBL-producing and AmpC-producing E. coli isolates, respectively. The presence of the same conjugative plasmids was found in genetic diversity ESC-resistant E. coli colonies collected on different sampling days. Our study emphasizes that cross-contamination of ESBL/AmpC-producing E. coli in slaughterhouse has a crucial impact on the occurrence of ESC resistance in retail chicken meat. [ABSTRACT FROM AUTHOR]