Transmission dynamics of carbapenemase-producing Gram-negative bacteria and mobile genetic elements between hospital and household settings in Benin

Carbapenems are last resort antibiotics in the healthcare system today. Unfortunately, during hospitalization patients can acquire and become colonised by carbapenemase-producing Gram-negative bacteria, which may be further transmitted to household contacts after discharge. The present study aimed to assess the transmission of carbapenem-resistant organisms (CROs) from hospitals to households through patients and their caregivers. A total of 248 participants were included in this study across 5 hospitals, comprising 81 index patients, 81 caregivers, 58 healthcare workers, and 28 household members. Rectal swabs samples were collected from the participants from admission to discharge and during follow-up at home. Samples were plated on mSuperCARBA™, and obtained isolates were tested for carbapenem resistance. A subset of 41 carbapenem resistant isolates was selected and subjected to Whole Genome Sequencing (WGS) and hybrid assembly analysis to determine genetic relatedness and resistance determinants across sampling networks. A total of 141 carbapenem-resistant isolates, predominantly E. coli (40.4%), Klebsiella pneumoniae (19.1%), and Acinetobacter baumannii (10.6%), were recovered from rectal swab samples collected from hospital and household settings. For those enrolled at a hospital, the prevalence of carbapenem-resistant bacterial colonization increased from 7.3% (16/220; 95% CI: 4.5–11.5) at admission to 22.7% (10/44; 95% CI: 12.8–37.0) by day 8 of hospitalization. Among patients or caregivers that were still positive at discharge, the prevalence at home rose from 8.0% (7/87; 95% CI: 4.0–15.7) on day 0 of discharge to 57.1% (8/14; 95% CI: 32.6–78.6) by day 14 of follow-up. Long- and short-read sequencing identified the carbapenem resistance genes blaNDM-5 and blaNDM-1 as the main determinants found in E. coli ST410 and K. pneumoniae ST147, respectively. Several strains, including K. pneumoniae (ST147) and E. coli (ST410), showed genetic relatedness and potential transmission within households and between healthcare and home settings. Inc FII and Inc FI conjugative plasmids carried most carbapenemase genes in addition to a multitude of other antimicrobial resistance genes in healthcare and community settings representing another layer of resistance spread via horizontal gene transfer. This study reveals, for the first time in Benin, the role of patients and their caregivers in facilitating the spread of antimicrobial resistance between hospitals and the community.