Comparing the transmission of carbapenemase-producing and extended-spectrum beta-lactamase-producing Escherichia coli between broiler chickens

Natcha Dankittipong; Jesse B Alderliesten; Jan Van den Broek; M Anita Dame-Korevaar; Michael S M Brouwer; Francisca C Velkers; Alex Bossers; Clazien J de Vos; Jaap A Wagenaar; J Arjan Stegeman; Egil A J Fischer

doi:10.1016/j.prevetmed.2023.105998

Comparing the transmission of carbapenemase-producing and extended-spectrum beta-lactamase-producing Escherichia coli between broiler chickens

Prev Vet Med. 2023 Oct:219:105998. doi: 10.1016/j.prevetmed.2023.105998. Epub 2023 Aug 17.

Affiliations

¹ Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, Utrecht, the Netherlands.
² Wageningen Bioveterinary Research, Wageningen University & Research, Houtribweg 39, Lelystad, the Netherlands.
³ Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, Utrecht, the Netherlands; Wageningen Bioveterinary Research, Wageningen University & Research, Houtribweg 39, Lelystad, the Netherlands.
⁴ Faculty of Veterinary Medicine, Utrecht University, Yalelaan 7, Utrecht, the Netherlands. Electronic address: E.A.J.fischer@uu.nl.

PMID: 37647719
DOI: 10.1016/j.prevetmed.2023.105998

Abstract

The emergence of carbapenemase-producing Enterobacteriaceae (CPE) is a threat to public health, because of their resistance to clinically important carbapenem antibiotics. The emergence of CPE in meat-producing animals is particularly worrying because consumption of meat contaminated with resistant bacteria comparable to CPE, such as extended-spectrum beta-lactamase (ESBL)-producing Enterobacteriaceae, contributed to colonization in humans worldwide. Currently, no data on the transmission of CPE in livestock is available. We performed a transmission experiment to quantify the transmission of CPE between broilers to fill this knowledge gap and to compare the transmission rates of CPE and other antibiotic-resistant E. coli. A total of 180 Ross 308 broiler chickens were distributed over 12 pens on the day of hatch (day 0). On day 5, half of the 10 remaining chickens in each pen were orally inoculated with 5·10² colony-forming units of CPE, ESBL, or chloramphenicol-resistant E. coli (catA1). To evaluate the effect of antibiotic treatment, amoxicillin was given twice daily in drinking water in 6 of the 12 pens from days 2-6. Cloacal swabs of all animals were taken to determine the number of infectious broilers. We used a Bayesian hierarchical model to quantify the transmission of the E. coli strains. E. coli can survive in the environment and serve as a reservoir. Therefore, the susceptible-infectious transmission model was adapted to account for the transmission of resistant bacteria from the environment. In addition, the caecal microbiome was analyzed on day 5 and at the end of the experiment on day 14 to assess the relationship between the caecal microbiome and the transmission rates. The transmission rates of CPE were 52 - 68 per cent lower compared to ESBL and catA1, but it is not clear if these differences were caused by differences between the resistance genes or by other differences between the E. coli strains. Differences between the groups in transmission rates and microbiome diversity did not correspond to each other, indicating that differences in transmission rates were probably not caused by major differences in the community structure in the caecal microbiome. Amoxicillin treatment from day 2-6 increased the transmission rate more than three-fold in all inoculums. It also increased alpha-diversity compared to untreated animals on day 5, but not on day 14, suggesting only a temporary effect. Future research could incorporate more complex transmission models with different species of resistant bacteria into the Bayesian hierarchical model.

Keywords: Antibiotic treatment; Bayesian inference; Carbapenem-resistant Enterobacteriaceae; Extended-spectrum beta-lactamase; Indirect transmission; Microbiome analysis.