TY - JOUR

T1 - NDM-1- and OXA-23-producing Acinetobacter baumannii in wastewater of a Nigerian hospital

AU - Odih, Erkison Ewomazino

AU - Sunmonu, Gabriel Temitope

AU - Okeke, Iruka N.

AU - Dalsgaard, Anders

N1 - Publisher Copyright: Copyright © 2023 Odih et al.

PY - 2023

Y1 - 2023

N2 - Carbapenem-resistant Acinetobacter baumannii spp. are increasingly important pathogens with limited treatment options, and there is limited knowledge on the environmental factors contributing to their spread. We determined the occurrence of carbapenem-resistant A. baumannii in hospital wastewater and their phylogenetic relationships with clinical A. baumannii isolates. Grab samples of raw and treated hospital wastewater were collected monthly at the University College Hospital, Ibadan, Nigeria, between March 2021 and February 2022. Acinetobacter baumannii strains were selectively isolated and identified using VITEK2, and their whole genomes were sequenced on an Illumina platform. We performed antimicrobial susceptibility testing and in silico genomic characterization of the strains and determined their phylogenetic relationships to previously characterized clinical A. baumannii strains from Nigeria. A. baumannii complex isolates were recovered from wastewater throughout the study. Of the 82 isolates identified based on whole-genome sequences, 77 were A. baumannii. A. baumannii isolates had high resistance rates (≥48.1%) to 10 of 12 antimicrobials tested, and majority (42/77, 54.5%) were resistant to carbapenems, with blaNDM-1 being the most common (24/77, 31.2%) carbapenem resistance gene detected, followed by blaOXA-23 (n = 22, 28.6%). There was no statistically significant difference in carbapenem resistance rates or carbapenem gene carriage between the raw and treated wastewater isolates. Most of the isolates belonged to novel or sparsely described lineages, some of which were closely related to clinical isolates. The release of inadequately treated hospital wastewater into the environment may contribute to the increased spread of carbapenem-resistant and clinically important A. baumannii lineages in Ibadan, Nigeria. IMPORTANCE Acinetobacter baumannii is a leading cause of hospital-associated infections globally. A. baumannii reservoirs outside hospital settings are still unknown, and their occurrence in the environment is linked to clinical and anthropogenic activities. Although the risk of transmission of A. baumannii from environmental sources to humans is not fully understood, these sources pose significant risks for the continued dissemination of A. baumannii and their resistance traits. This study provides evidence that diverse and clinically relevant A. baumannii strains, many of which are resistant to carbapenems, are constantly being discharged into the environment through inadequately treated hospital wastewater. We further elucidate potential transmission routes between the environment and clinical infections and demonstrate the high prevalence of carbapenem resistance genes on highly mobile transposons among these strains. Our findings highlight the pressing need to address hospital wastewater as a crucial factor in curtailing the spread of carbapenem-resistant A. baumannii.

AB - Carbapenem-resistant Acinetobacter baumannii spp. are increasingly important pathogens with limited treatment options, and there is limited knowledge on the environmental factors contributing to their spread. We determined the occurrence of carbapenem-resistant A. baumannii in hospital wastewater and their phylogenetic relationships with clinical A. baumannii isolates. Grab samples of raw and treated hospital wastewater were collected monthly at the University College Hospital, Ibadan, Nigeria, between March 2021 and February 2022. Acinetobacter baumannii strains were selectively isolated and identified using VITEK2, and their whole genomes were sequenced on an Illumina platform. We performed antimicrobial susceptibility testing and in silico genomic characterization of the strains and determined their phylogenetic relationships to previously characterized clinical A. baumannii strains from Nigeria. A. baumannii complex isolates were recovered from wastewater throughout the study. Of the 82 isolates identified based on whole-genome sequences, 77 were A. baumannii. A. baumannii isolates had high resistance rates (≥48.1%) to 10 of 12 antimicrobials tested, and majority (42/77, 54.5%) were resistant to carbapenems, with blaNDM-1 being the most common (24/77, 31.2%) carbapenem resistance gene detected, followed by blaOXA-23 (n = 22, 28.6%). There was no statistically significant difference in carbapenem resistance rates or carbapenem gene carriage between the raw and treated wastewater isolates. Most of the isolates belonged to novel or sparsely described lineages, some of which were closely related to clinical isolates. The release of inadequately treated hospital wastewater into the environment may contribute to the increased spread of carbapenem-resistant and clinically important A. baumannii lineages in Ibadan, Nigeria. IMPORTANCE Acinetobacter baumannii is a leading cause of hospital-associated infections globally. A. baumannii reservoirs outside hospital settings are still unknown, and their occurrence in the environment is linked to clinical and anthropogenic activities. Although the risk of transmission of A. baumannii from environmental sources to humans is not fully understood, these sources pose significant risks for the continued dissemination of A. baumannii and their resistance traits. This study provides evidence that diverse and clinically relevant A. baumannii strains, many of which are resistant to carbapenems, are constantly being discharged into the environment through inadequately treated hospital wastewater. We further elucidate potential transmission routes between the environment and clinical infections and demonstrate the high prevalence of carbapenem resistance genes on highly mobile transposons among these strains. Our findings highlight the pressing need to address hospital wastewater as a crucial factor in curtailing the spread of carbapenem-resistant A. baumannii.

KW - antimicrobial resistance

KW - carbapenem resistance

KW - carbapenem-resistant Acinetobacter baumannii

KW - hospital wastewater

KW - international clone

U2 - 10.1128/spectrum.02381-23

DO - 10.1128/spectrum.02381-23

M3 - Journal article

C2 - 37796014

AN - SCOPUS:85180270964

VL - 11

JO - Microbiology spectrum

JF - Microbiology spectrum

SN - 2165-0497

IS - 6

M1 - e02381-23

ER -