Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh
Antibiotic resistance is a leading cause of hospitalization and death worldwide. Heavy metals such as arsenic have been shown to drive co-selection of antibiotic resistance, suggesting arsenic-contaminated drinking water is a risk factor for antibiotic resistance carriage. This study aimed to determ...
| Main Authors: | , , , , , , , , , , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2022-12-01
|
| Series: | PLoS Pathogens |
| Online Access: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9731454/?tool=EBI |
| _version_ | 1828113810859229184 |
|---|---|
| author | Mohammed Badrul Amin Prabhat Kumar Talukdar Muhammad Asaduzzaman Subarna Roy Brandon M. Flatgard Md. Rayhanul Islam Sumita Rani Saha Zahid Hayat Mahmud Tala Navab-Daneshmand Molly L. Kile Karen Levy Timothy R. Julian Mohammad Aminul Islam |
| author_facet | Mohammed Badrul Amin Prabhat Kumar Talukdar Muhammad Asaduzzaman Subarna Roy Brandon M. Flatgard Md. Rayhanul Islam Sumita Rani Saha Zahid Hayat Mahmud Tala Navab-Daneshmand Molly L. Kile Karen Levy Timothy R. Julian Mohammad Aminul Islam |
| author_sort | Mohammed Badrul Amin |
| collection | DOAJ |
| description | Antibiotic resistance is a leading cause of hospitalization and death worldwide. Heavy metals such as arsenic have been shown to drive co-selection of antibiotic resistance, suggesting arsenic-contaminated drinking water is a risk factor for antibiotic resistance carriage. This study aimed to determine the prevalence and abundance of antibiotic-resistant Escherichia coli (AR-Ec) among people and drinking water in high (Hajiganj, >100 μg/L) and low arsenic-contaminated (Matlab, <20 μg/L) areas in Bangladesh. Drinking water and stool from mothers and their children (<1 year) were collected from 50 households per area. AR-Ec was detected via selective culture plating and isolates were tested for antibiotic resistance, arsenic resistance, and diarrheagenic genes by PCR. Whole-genome sequencing (WGS) analysis was done for 30 E. coli isolates from 10 households. Prevalence of AR-Ec was significantly higher in water in Hajiganj (48%) compared to water in Matlab (22%, p <0.05) and among children in Hajiganj (94%) compared to children in Matlab (76%, p <0.05), but not among mothers. A significantly higher proportion of E. coli isolates from Hajiganj were multidrug-resistant (83%) compared to isolates from Matlab (71%, p <0.05). Co-resistance to arsenic and multiple antibiotics (MAR index >0.2) was observed in a higher proportion of water (78%) and child stool (100%) isolates in Hajiganj than in water (57%) and children (89%) in Matlab (p <0.05). The odds of arsenic-resistant bacteria being resistant to third-generation cephalosporin antibiotics were higher compared to arsenic-sensitive bacteria (odds ratios, OR 1.2–7.0, p <0.01). WGS-based phylogenetic analysis of E. coli isolates did not reveal any clustering based on arsenic exposure and no significant difference in resistome was found among the isolates between the two areas. The positive association detected between arsenic exposure and antibiotic resistance carriage among children in arsenic-affected areas in Bangladesh is an important public health concern that warrants redoubling efforts to reduce arsenic exposure. Author summary Antibiotic resistance is one of the leading causes of death and hospitalization worldwide. While the major drivers of antibiotic resistance are the overuse and misuse of antibiotics, natural elements such as heavy metals can also promote antibiotic resistance. In this observational study, we investigated the prevalence and abundance of antibiotic-resistant bacteria in drinking water samples and among mothers and children from the same households in two rural areas of Bangladesh with high and low levels of arsenic contamination in drinking water. We found that the prevalence of antibiotic-resistant E. coli was significantly higher in water and among children in high arsenic-contaminated areas compared to the low arsenic-contaminated areas. We also found that a higher proportion of E. coli isolates from the high arsenic area were resistant to multiple antibiotics including penicillin, cephalosporin, and chloramphenicol. Arsenic-resistant bacteria are more likely to be resistant to certain groups of antibiotics, including third-generation cephalosporins. Overall, this study suggests that arsenic exposure could be an important risk factor for the carriage of antibiotic-resistant organisms which needs to be taken into consideration when designing community-based interventions to combat antimicrobial resistance. |
| first_indexed | 2024-04-11T12:16:04Z |
| format | Article |
| id | doaj.art-5c0a5ed5103a4b98b76631ed879cd9de |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-04-11T12:16:04Z |
| publishDate | 2022-12-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-5c0a5ed5103a4b98b76631ed879cd9de2022-12-22T04:24:19ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742022-12-011812Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural BangladeshMohammed Badrul AminPrabhat Kumar TalukdarMuhammad AsaduzzamanSubarna RoyBrandon M. FlatgardMd. Rayhanul IslamSumita Rani SahaZahid Hayat MahmudTala Navab-DaneshmandMolly L. KileKaren LevyTimothy R. JulianMohammad Aminul IslamAntibiotic resistance is a leading cause of hospitalization and death worldwide. Heavy metals such as arsenic have been shown to drive co-selection of antibiotic resistance, suggesting arsenic-contaminated drinking water is a risk factor for antibiotic resistance carriage. This study aimed to determine the prevalence and abundance of antibiotic-resistant Escherichia coli (AR-Ec) among people and drinking water in high (Hajiganj, >100 μg/L) and low arsenic-contaminated (Matlab, <20 μg/L) areas in Bangladesh. Drinking water and stool from mothers and their children (<1 year) were collected from 50 households per area. AR-Ec was detected via selective culture plating and isolates were tested for antibiotic resistance, arsenic resistance, and diarrheagenic genes by PCR. Whole-genome sequencing (WGS) analysis was done for 30 E. coli isolates from 10 households. Prevalence of AR-Ec was significantly higher in water in Hajiganj (48%) compared to water in Matlab (22%, p <0.05) and among children in Hajiganj (94%) compared to children in Matlab (76%, p <0.05), but not among mothers. A significantly higher proportion of E. coli isolates from Hajiganj were multidrug-resistant (83%) compared to isolates from Matlab (71%, p <0.05). Co-resistance to arsenic and multiple antibiotics (MAR index >0.2) was observed in a higher proportion of water (78%) and child stool (100%) isolates in Hajiganj than in water (57%) and children (89%) in Matlab (p <0.05). The odds of arsenic-resistant bacteria being resistant to third-generation cephalosporin antibiotics were higher compared to arsenic-sensitive bacteria (odds ratios, OR 1.2–7.0, p <0.01). WGS-based phylogenetic analysis of E. coli isolates did not reveal any clustering based on arsenic exposure and no significant difference in resistome was found among the isolates between the two areas. The positive association detected between arsenic exposure and antibiotic resistance carriage among children in arsenic-affected areas in Bangladesh is an important public health concern that warrants redoubling efforts to reduce arsenic exposure. Author summary Antibiotic resistance is one of the leading causes of death and hospitalization worldwide. While the major drivers of antibiotic resistance are the overuse and misuse of antibiotics, natural elements such as heavy metals can also promote antibiotic resistance. In this observational study, we investigated the prevalence and abundance of antibiotic-resistant bacteria in drinking water samples and among mothers and children from the same households in two rural areas of Bangladesh with high and low levels of arsenic contamination in drinking water. We found that the prevalence of antibiotic-resistant E. coli was significantly higher in water and among children in high arsenic-contaminated areas compared to the low arsenic-contaminated areas. We also found that a higher proportion of E. coli isolates from the high arsenic area were resistant to multiple antibiotics including penicillin, cephalosporin, and chloramphenicol. Arsenic-resistant bacteria are more likely to be resistant to certain groups of antibiotics, including third-generation cephalosporins. Overall, this study suggests that arsenic exposure could be an important risk factor for the carriage of antibiotic-resistant organisms which needs to be taken into consideration when designing community-based interventions to combat antimicrobial resistance.https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9731454/?tool=EBI |
| spellingShingle | Mohammed Badrul Amin Prabhat Kumar Talukdar Muhammad Asaduzzaman Subarna Roy Brandon M. Flatgard Md. Rayhanul Islam Sumita Rani Saha Zahid Hayat Mahmud Tala Navab-Daneshmand Molly L. Kile Karen Levy Timothy R. Julian Mohammad Aminul Islam Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh PLoS Pathogens |
| title | Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh |
| title_full | Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh |
| title_fullStr | Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh |
| title_full_unstemmed | Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh |
| title_short | Effects of chronic exposure to arsenic on the fecal carriage of antibiotic-resistant Escherichia coli among people in rural Bangladesh |
| title_sort | effects of chronic exposure to arsenic on the fecal carriage of antibiotic resistant escherichia coli among people in rural bangladesh |
| url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9731454/?tool=EBI |
| work_keys_str_mv | AT mohammedbadrulamin effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT prabhatkumartalukdar effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT muhammadasaduzzaman effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT subarnaroy effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT brandonmflatgard effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT mdrayhanulislam effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT sumitaranisaha effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT zahidhayatmahmud effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT talanavabdaneshmand effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT mollylkile effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT karenlevy effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT timothyrjulian effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh AT mohammadaminulislam effectsofchronicexposuretoarseniconthefecalcarriageofantibioticresistantescherichiacoliamongpeopleinruralbangladesh |