Carbapenem Resistance in Animal-Environment-Food from Africa: A Systematic Review, Recommendations and Perspectives

Abstract

Background The World Health Organization (WHO) has classified carbapenem-resistant Enterobacteriaceae, Pseudomonas aeruginosa ( P. aeruginosa ), and Acinetobacter baumannii ( A. baumannii ) as high-priority pathogens, and carbapenem-resistant bacteria (CRB) have been reported to spread between humans, animals, and the environment. Objective This study aimed to conduct a systematic review of carbapenem resistance in animals, foods, and the environment on the African continent and to provide recommendations and perspectives for better prevention and control of carbapenem resistance in Africa. Results A total of 137 research articles collected from 2009 to 2023 were selected for this review, including articles reporting carbapenem-resistant bacteria in animals (81/137; 59.1%), the environment (66/137; 48.2%), and foods (26/137; 19%). Carbapenem-resistant bacterial species belonged to 31 genera and 17 families, including mainly Escherichia spp. (68/127; 53.5%); Klebsiella spp. (45/127; 35.4%); Pseudomonas spp. (20/127; 15.7%), Enterobacter spp. (19/127; 15%) and Acinetobacter spp. (15/127; 11.8%). The prevalence of CRBs by country ranged from 1.1% to 48.5%, and the pooled prevalence of CRBs isolated from animal-environment-food in Africa was 19.1% (2804/14,684; Standard Deviation = 15). Twenty carbapenemase families belonging to A, B, C, and D Ambler classes were reported, including mainly carbapenemase genes from bla OXA (44/84; 52.4%), bla NDM (34/84; 40.5%), bla SHV (23/84; 27.4%), bla KPC (22/84; 26.2%), bla VIM (19/84; 22.6%), and bla IMP (12/84; 14.3%) families. The reported mobile genetic elements (MGE) carrying carbapenemase-encoding genes included plasmids (16/19; 84.2%), integrons (3/19; 15.8%), transposons (3/19; 15.8%), and insertion sequences (2/19; 10.5%). bla OXA-48 was often carried by (60kb-65kb) IncL/M-type pOXA-48 plasmids, while bla NDM-5 was often carried by (45–50kb) IncX-type plasmids. Moreover, 25 articles investigated and reported virulent and hypervirulent CRBs that carried multiple virulence factors. Conclusion Animal-environment-food ecosystems would constitute reservoirs of CRBs involved in human infections. The One Health approach and constant collaboration between governments are necessary to drastically reduce the mortality rates linked to antimicrobial resistance.