Skip to main page content
U.S. flag

An official website of the United States government

Dot gov

The .gov means it’s official.
Federal government websites often end in .gov or .mil. Before sharing sensitive information, make sure you’re on a federal government site.

Https

The site is secure.
The https:// ensures that you are connecting to the official website and that any information you provide is encrypted and transmitted securely.

Access keys NCBI Homepage MyNCBI Homepage Main Content Main Navigation
. 2022 Apr 7:12:869314.
doi: 10.3389/fcimb.2022.869314. eCollection 2022.

Extended-Spectrum ß-Lactamase-Producing Escherichia coli Among Humans, Beef Cattle, and Abattoir Environments in Nigeria

Mabel Kamweli Aworh  1   2 , Eme Ekeng  3 , Pernille Nilsson  4 , Beverly Egyir  5 , Christian Owusu-Nyantakyi  5 , Rene S Hendriksen  4
Affiliations

Extended-Spectrum ß-Lactamase-Producing Escherichia coli Among Humans, Beef Cattle, and Abattoir Environments in Nigeria

Mabel Kamweli Aworh et al. Front Cell Infect Microbiol. .

Abstract

Introduction: Beef cattle, one of the food-producing animals, are linked to humans through a shared environment and the food chain as a major source of animal protein. Antimicrobial drugs are readily accessible for use in food animal production in Nigeria. Beef cattle and abattoir environments harbor pathogenic bacteria such as Escherichia coli (E. coli) which have developed resistance to antimicrobial agents used for prophylaxis or treatment. This study investigated the zoonotic transmission of extended-spectrum beta-lactamase-producing E. coli (ESBL-EC) among humans, beef cattle, and abattoir environments in Abuja and Lagos, Nigeria.

Materials and methods: We conducted a cross-sectional study among abattoir workers, beef cattle, and abattoir environments in Abuja and Lagos. Stool, cecal, and environmental samples were collected from apparently healthy workers, slaughtered cattle, and abattoir environments from May to December 2020. Data were collected electronically using open data kit app installed on a mobile phone. Antimicrobial susceptibility patterns were determined using the Kirby-Bauer disk diffusion method against a panel of 16 antimicrobial agents. Phenotypic and genotypic characterizations of the isolates were conducted. Data were analyzed with descriptive statistics.

Results: From 21.7% (n = 97) of 448 samples, ESBL-EC were isolated and further characterized. Prevalence of ESBL-EC was highest in cattle (45.4%; n = 44), abattoir workers (41.2%; n = 40), and abattoir environment (13.4%; n = 13). Whole-genome sequencing of ESBL-EC showed dissemination of blaCTX-M-15 (90.7%; n = 88); blaCTX-M-14 (5.2%; n = 5); and blaCTX-M-55 (2.1%; n = 2) genes. The blaCTX-M-15 coexisted with blaCTX-M-14 and blaTEM-1 genes in 2.1% (n = 2) and 39.2% (n = 38) of the isolates, respectively. The presence of blaCTX-M-14 and blaCTX-M-15 genes was significantly associated with isolates originating from abattoir workers when compared with beef cattle isolates (p = 0.05; p < 0.01). The most prevalent sequence types (ST) were ST10 (n = 11), ST215 (n = 7), ST4684 (n = 7), and ST2178 (n = 6). ESBL-EC strain (ST205/B1) harbored mcr-1.1 and blaCTX-M15 and was isolated from a worker at Lagos abattoir. In 91 ESBL-EC isolates, 219 mobile genetic elements (MGEs) harbored resistance genes out of which β-lactam genes were carried on 64 different MGEs. Isolates showed equal distribution of insertion sequences and miniature inverted repeats although only a few composite transposons were detected (humans n = 12; cattle n = 9; environment n = 4). Two isolates of human and cattle origin (ST46/A) harboring ESBL genes and carried by MGEs were clonally related.

Conclusions: This is the first report of blaCTX-M-55 gene in humans and cattle in Nigeria. This study demonstrates the horizontal transfer of ESBL genes possibly by MGEs and buttresses the importance of genomic surveillance. Healthcare workers should be sensitized that people working closely with cattle or in abattoir environments are a high-risk group for fecal carriage of ESBL-EC when compared with the general population.

Keywords: Escherichia coli; Nigeria; abattoir; antimicrobial; cattle; environment; resistance.

PubMed Disclaimer

Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Figure 1
Figure 1
Prevalence of ESBL-EC isolated from humans, cattle, and abattoir environments in Abuja and Lagos Nigeria, 2021. Bars represent the proportion of ESBL-EC isolates from each isolation source with 95% confidence intervals. Error bars represent standard error of the mean prevalence. Data were obtained from two sources: Abuja and Lagos abattoirs.
Figure 2
Figure 2
Resistance determinants detected in ESBL-EC isolates from humans, cattle, and abattoir environments in Abuja and Lagos—Nigeria. Each bar represents the various antimicrobial-resistant genes detected in ESBL-EC isolates obtained from abattoir workers, beef cattle, and abattoir environments.
Figure 3
Figure 3
Multilocus sequence types for ESBL-EC isolated from humans, beef cattle, and abattoir environments in Abuja and Lagos—Nigeria. Each bar represents the various ESBL-EC sequence types for isolates obtained from abattoir workers, beef cattle, and abattoir environments.
Figure 4
Figure 4
Total number of predicted MGEs in ESBL-EC isolates from all sources.
Figure 5
Figure 5
SNP-based phylogeny of ESBL E. coli isolates from humans, cattle, and abattoir environments in Abuja and Lagos. SNP-based maximum likelihood phylogeny of E. coli isolates visualized in iterative Tree of life tool (iTol). The tree was rooted in a reference isolate E. coli strain NCTC11129. Clustering of isolates was found to be following the core genome and SNP-based phylogenies. The clustering of isolates belonging to the same phylogenetic group and sequence type was consistent. Shown for each isolate is the source: humans, cattle or environment, location, phylogroup, sequence types (STs), AMR genes and plasmid replicons, and number of MGEs.
See this image and copyright information in PMC

References

    1. Agyare C., Etsiapa Boamah V., Ngofi Zumbi C., Boateng Osei F. (2019). “Antibiotic Use in Poultry Production and Its Effects on Bacterial Resistance,” in Antimicrobial Resistance - A Global Threat (InTech Open Science; ) doi: 10.5772/intechopen.79371 - DOI
    1. Aworh M. K., Kwaga J., Okolocha E., Harden L., Hull D., Hendriksen R. S., et al. . (2020). Extended-Spectrum ß-Lactamase-Producing Escherichia Coli Among Humans, Chickens and Poultry Environments in Abuja, Nigeria. One Heal Outlook 2 (1), 8. doi: 10.1186/s42522-020-00014-7 - DOI - PMC - PubMed
    1. Aworh M. K., Kwaga J., Okolocha E., Mba N., Thakur S. (2019). Prevalence and Risk Factors for Multi-Drug Resistant Escherichia Coli Among Poultry Workers in the Federal Capital Territory, Abuja, Nigeria. PloS One 14 (11), 1–15. doi: 10.1371/journal.pone.0225379 - DOI - PMC - PubMed
    1. Beghain J., Bridier-Nahmias A., Nagard H., Denamur E., Clermont O. (2018). Clermontyping: An Easy-to-Use and Accurate In Silico Method for Escherichia Genus Strain Phylotyping. Microb. Genomics 4 (7), 1–8. doi: 10.1099/mgen.0.000192 - DOI - PMC - PubMed
    1. Bettencourt E. M. V., Tilman M., Narciso V., da Silva Carvalho M. L., de Sousa Henriques P. D. (2015). The Livestock Roles in the Wellbeing of Rural Communities of Timor-Leste. Rev. Econ e Sociol Rural 53, S063–S080. doi: 10.1590/1234-56781806-94790053s01005 - DOI

Publication types

MeSH terms