Metagenomic Analysis of the Abundance and Composition of Antibiotic Resistance Genes in Hospital Wastewater in Benin, Burkina Faso, and Finland

Markkanen, Melina; Haukka, Kaisa; Pärnänen, Katariina; Dougnon, Victorien; Bonkoungou, Isidore Juste O.; Garba, Zakaria; Tinto, Halidou; Sarekoski, Anniina; Karkman, Antti; Virta, Marko

doi:10.1128/msphere.00538-22

Cited by 26 publications

(17 citation statements)

References 79 publications

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“…The presence of ESBL-producing E. coli in hospital effluents is of particular concern. In this study, all E. coli isolates from hospital effluents were found to be ESBL producers, consistent with the findings of Markkanen et al ( 21 ), who identified hospital effluents as hotspots for ESBL genes. Similarly, Gumede et al ( 37 ) reported a high number of ESBL-producing E. coli in hospital wastewater in South Africa.…”

Section: Discussionsupporting

confidence: 92%

“…Although studies have reported the presence of ESBL-producing bacteria and their resistance genes in various samples from Africa and globally ( 7 , 20–23 ), limited data exist on the prevalence of ESBL-producing Enterobacterales in healthy pregnant women, the food chain, and the environment in Benin ( 21 , 24–28 ). Therefore, the present study investigates the prevalence and characteristics of ESBL-producing E. coli in healthy pregnant women, the hospital environment, and the food chain within various tertiary hospitals in Benin.…”

Section: Introductionmentioning

confidence: 99%

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Prevalence and characterization of ESBL-producing Escherichia coli in healthy pregnant women and hospital environments in Benin: an approach based on Tricycle

Sintondji,

Fabiyi,

Hougbenou

et al. 2023

Front. Public Health

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IntroductionExtended-Spectrum Beta-Lactamase (ESBL)-producing Enterobacterales are recognized as significant pathogens due to their resistance to multiple antibiotics. This study aimed to determine the prevalence of ESBL-producing Escherichia coli (E. coli) in different settings, including healthy pregnant women, the food chain, and the environment of tertiary hospitals in Benin.MethodsSamples were collected from various sources, including fecal samples from healthy pregnant women, food samples from hospital canteens, and hospital effluents from four tertiary hospitals in southern Benin. Fecal samples were plated on MacConkey agar supplemented with cefotaxime (4 μg/mL), while food and water samples were plated on Tryptone Bile X agar supplemented with cefotaxime (4 μg/mL). Urea indole tests were used for preliminary identification of E. coli colonies, followed by confirmation of ESBL production using the double disk synergy technique. Antibiotic susceptibility testing of ESBL-producing E. coli strains was conducted using the disk diffusion method on MH agar. Polymerase Chain Reaction (PCR) was used to investigate the presence of ESBL-encoding genes.ResultsAmong the 296 fecal samples collected from four tertiary hospitals, ESBL-producing E. coli was isolated from 22.30% (66) of the samples. All E. coli isolates from hospital effluents exhibited ESBL production, while ESBL-producing E. coli was not detected in food and drinking water samples. The analysis of variable associations showed no significant associations (p > 0.05) for the studied factors. Antibiotic susceptibility testing revealed high resistance rates among the ESBL-Ec isolates against several tested antibiotics, including amoxicillin, aztreonam, ceftriaxone, ciprofloxacin, and trimethoprim-sulfamethoxazole. However, most isolates remained susceptible to ertapenem, amoxicillin-clavulanate, and imipenem. The most prevalent ESBL-encoding genes were blaTEM (37.50%), blaOXA-1 (19.44%), and blaSHV (11.11%), while a smaller proportion of isolates carried blaCTXM-1/blaCTXM-15 (5.55%) and blaCTXM-9.DiscussionThis study provides insights into the prevalence of ESBL-producing E. coli carriage in the feces of healthy pregnant women in southern Benin. Additionally, it highlights hospital wastewater as a potential reservoir of ESBL-producing bacteria in the environment. The detection of ESBL-producing E. coli in hospital effluents raises concerns about the dissemination of antibiotic resistance genes into the environment. The high resistance rates observed among ESBL-Ec isolates against commonly used antibiotics emphasize the urgent need for antimicrobial stewardship and infection control measures. The identification of prevalent ESBL-encoding genes contributes to understanding the genetic basis of ESBL resistance in the studied population. Further research is warranted to explore the mechanisms of transmission and potential interventions to mitigate the spread of ESBL-producing Enterobacterales.

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Section: Discussionsupporting

confidence: 92%

Section: Introductionmentioning

confidence: 99%

Prevalence and characterization of ESBL-producing Escherichia coli in healthy pregnant women and hospital environments in Benin: an approach based on Tricycle

Sintondji,

Fabiyi,

Hougbenou

et al. 2023

Front. Public Health

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“…The frequency of fluoroquinolone genes in the category varied between 7.2% and 80.3%, where the qnrB-31 genes were found to have the highest frequencies. Markkanen et al ( 2022 ) discovered the carbapenemase genes blaKPC, blaNDM, blaIMP, blaOXA-48, and blaOXA-58 in hospital wastewater samples from Burkina Faso and Finland. It was believed that Acinetobacter baumannii , an opportunistic pathogen is known to cause nosocomial infections, was almost exclusively associated with the blaOXA-58, blaOXA-51, and blaOXA-23ARGgenes (Cacace et al 2019 ).…”

Section: Resultsmentioning

confidence: 99%

Adsorptive removal of levofloxacin and antibiotic resistance genes from hospital wastewater by nano-zero-valent iron and nano-copper using kinetic studies and response surface methodology

Hamad

El-Sesy

2023

Bioresour. Bioprocess.

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In the twenty-first century, water contamination with pharmaceutical residues is becoming a global phenomenon and a threat. Antibiotic residues and antibiotic resistance genes (ARGs) are recognized as new emerging water pollutants because they can negatively affect aquatic ecosystems and human health, thereby posing a complex environmental problem. These nano-adsorbents of the next generation can remove these pollutants at low concentrations. This study focuses on the chemical synthesis of copper oxide nanoparticles (CuONPs) and nano-zero-valent iron (nZVI) used as nano-adsorbents for levofloxacin removal from water samples and antibiotic-resistant genes. The CuONPs and nZVI are initially characterized by transmission electron microscopy, scanning electron microscopy, and X-ray diffraction. The levofloxacin adsorption isotherm on the CuONPS and nZVI shows the best fit with the Langmuir isotherm model, exhibiting correlation coefficients (R2) of 0.993 and 0.999, respectively. The adsorption activities of CuONPS and nZVI were fitted to a pseudo-second-order kinetic model with correlation coefficients (R2) of 0.983 and 0.994, respectively. The maximum levofloxacin removal capacity was observed at (89%), (84%), (89%), (88%) and (71.6) at pH 7 and adsorbent dose(0.06 mg/L), initial LEV concentration (1 mg/L), temperature 25 °C, and contact time 120 min for CuONPs. Removal efficiency was (91%), (90.6%), (91%), (89%), and (80%), at pH 7, adsorbent dose(0.06), initial LEV concentration (1 mg/L), temperature 35 °C, and contact time 120 min. The levofloxacin adsorption is an exothermic process for nZVI and CuONPs, according to thermodynamic analysis. A thermodynamic analysis indicated that each adsorption process is spontaneous. Several genera, including clinically pathogenic bacteria (e.g., Acinetobacter_baumannii, Helicobacter_pylori, Escherichia_coli, Pseudomonas_aeruginosa, Clostridium_beijerinckii, Escherichia/Shigella_coli, Helicobacter_cetorum, Lactobacillus_gasseri, Bacillus_cereus, Deinococcus_radiodurans, Rhodobacter_sphaeroides, Propionibacterium_acnes, and Bacteroides_vulgatus) were relatively abundant in hospital wastewater. Furthermore, 37 antibiotic resistance genes (ARGs) were quantified in hospital wastewater. The results demonstrated that 95.01% of nZVI and 91.4% of CuONPs are effective adsorbents for removing antibiotic-resistant bacteria from hospital effluent. The synthesized nZVI and CuONPs have excellent reusability and can be considered cost effective and eco-friendly adsorbents. Graphical Abstract

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“… (6) Brucella spp. (18) Burkina- Faso 2015 Wastewater used for urban agriculture Comamonadaceae, Chroococcaceae, Streptococcaceae, Enterobacteriaceae, Enterococcaceae, Staphylococcaceae NA bla OXA-226 , bla OXA-256 , bla OXA-347 , bla OXA-46 , bla SHV-100 , bla GES-21 , bla OXA-256 , (multiple virulence genes) NA [ 54 ] 2019 Hospital Wastewater A. baumannii NA bla OXA-58 , bla OXA-46 , bla CMY-2 , bla OXA-101 , bla OXA-56 , bla OXA-397 , bla OXA-48 , bla IMP , bla NDM , bla VIM , bla GES NA [ 50 ] 2019–2021 Wastewater from healthcare centers E. coli 35/107 (32.71) NDM, OXA-48 NA [ 55 ] K. pneumoniae 11/60 (18.33) Chad 2016–2018 Household meals, fresh milk, fresh meat, fresh fish, fresh vegetables E. coli, S. aureus 6/48 (12.5) NA NA [ 56 ] NA Fresh vegetables and fruits E. coli, S. aureus 6/60 (10) NA NA …”

Section: Resultsmentioning

confidence: 99%

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

Dossouvi,

Ametepe

2024

IDR

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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.

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Metagenomic Analysis of the Abundance and Composition of Antibiotic Resistance Genes in Hospital Wastewater in Benin, Burkina Faso, and Finland

Cited by 26 publications

References 79 publications

Prevalence and characterization of ESBL-producing Escherichia coli in healthy pregnant women and hospital environments in Benin: an approach based on Tricycle

Prevalence and characterization of ESBL-producing Escherichia coli in healthy pregnant women and hospital environments in Benin: an approach based on Tricycle

Adsorptive removal of levofloxacin and antibiotic resistance genes from hospital wastewater by nano-zero-valent iron and nano-copper using kinetic studies and response surface methodology

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

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