Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil
A growing concern regarding the use of animal manure as fertilizer is the contamination of soil, plants, and the environment with a variety of antibiotic-resistant and pathogenic bacteria. This study quantified and characterized the antibiotic resistance profiles of Escherichia coli in soil before a...
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2022-01-01
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| Series: | Frontiers in Environmental Science |
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| Online Access: | https://www.frontiersin.org/articles/10.3389/fenvs.2021.751732/full |
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| author | Dorcas Oladayo Fatoba Daniel Gyamfi Amoako Daniel Gyamfi Amoako Akebe Luther King Abia Sabiha Yusuf Essack |
| author_facet | Dorcas Oladayo Fatoba Daniel Gyamfi Amoako Daniel Gyamfi Amoako Akebe Luther King Abia Sabiha Yusuf Essack |
| author_sort | Dorcas Oladayo Fatoba |
| collection | DOAJ |
| description | A growing concern regarding the use of animal manure as fertilizer is the contamination of soil, plants, and the environment with a variety of antibiotic-resistant and pathogenic bacteria. This study quantified and characterized the antibiotic resistance profiles of Escherichia coli in soil before and after chicken litter application to determine the impact of manure on the soil resistome. Litter and soil samples were collected from a sugarcane field before and after litter application. E. coli was isolated and quantified using the Colilert®-18/Quanti-tray® 2000 and 10 randomly selected isolates from the positive wells of each Quanti-tray were putatively identified on eosin methylene blue agar. Real-time PCR was used to confirm the isolates by targeting the uidA gene. Antibiotic susceptibility test against 18 antibiotics was conducted using the disk diffusion method, and the multiple antibiotic resistance index was calculated. Soil amendment with chicken litter significantly increased the number of antibiotic-resistant E. coli in the soil. Among the 126 E. coli isolates purified from all the samples, 76% showed resistance to at least one antibiotic, of which 54.2% were multidrug-resistant (MDR). The highest percentage resistance was to tetracycline (78.1%), with the least percentage resistance (3.1%) to imipenem, tigecycline, and gentamicin. The isolates also showed resistance to chloramphenicol (63.5%), ampicillin (58.3%), trimethoprim-sulfamethoxazole (39.6%), cefotaxime (30.2%), ceftriaxone (26.0%), cephalexin (20.8%), cefepime (11.5%), amoxicillin-clavulanic acid (11.5%), cefoxitin (10.4%), Nalidixic acid (9.4%), amikacin (6.3%), and ciprofloxacin (4.2%). Of the 54.2% (52/96) MDR, the highest number was isolated from the litter-amended soil (61.5%) and the least isolates from soil samples collected before litter application (1.9%). The relatively higher mean MAR index of the litter-amended soil (0.14), compared to the soil before the amendment (0.04), suggests soil pollution with antibiotic-resistant E. coli from sources of high antibiotic use. E. coli could only be detected in the soil up to 42 days following manure application, making it a suitable short-term indicator of antibiotic resistance contamination. Notwithstanding its relatively short detectability/survival, the application of chicken litter appeared to transfer antibiotic-resistant E. coli to the soil, enhancing the soil resistome and highlighting the consequences of such agricultural practices on public health. |
| first_indexed | 2024-12-24T01:21:30Z |
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| id | doaj.art-2ded4b0bc5524034a1c700aa5d53b4cd |
| institution | Directory Open Access Journal |
| issn | 2296-665X |
| language | English |
| last_indexed | 2024-12-24T01:21:30Z |
| publishDate | 2022-01-01 |
| publisher | Frontiers Media S.A. |
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| series | Frontiers in Environmental Science |
| spelling | doaj.art-2ded4b0bc5524034a1c700aa5d53b4cd2022-12-21T17:22:38ZengFrontiers Media S.A.Frontiers in Environmental Science2296-665X2022-01-01910.3389/fenvs.2021.751732751732Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural SoilDorcas Oladayo Fatoba0Daniel Gyamfi Amoako1Daniel Gyamfi Amoako2Akebe Luther King Abia3Sabiha Yusuf Essack4Antimicrobial Research Unit, College of Health Science, University of KwaZulu-Natal, Durban, South AfricaAntimicrobial Research Unit, College of Health Science, University of KwaZulu-Natal, Durban, South AfricaSequencing Core Facility, National Health Laboratory Service, National Institute for Communicable Diseases, Johannesburg, South AfricaAntimicrobial Research Unit, College of Health Science, University of KwaZulu-Natal, Durban, South AfricaAntimicrobial Research Unit, College of Health Science, University of KwaZulu-Natal, Durban, South AfricaA growing concern regarding the use of animal manure as fertilizer is the contamination of soil, plants, and the environment with a variety of antibiotic-resistant and pathogenic bacteria. This study quantified and characterized the antibiotic resistance profiles of Escherichia coli in soil before and after chicken litter application to determine the impact of manure on the soil resistome. Litter and soil samples were collected from a sugarcane field before and after litter application. E. coli was isolated and quantified using the Colilert®-18/Quanti-tray® 2000 and 10 randomly selected isolates from the positive wells of each Quanti-tray were putatively identified on eosin methylene blue agar. Real-time PCR was used to confirm the isolates by targeting the uidA gene. Antibiotic susceptibility test against 18 antibiotics was conducted using the disk diffusion method, and the multiple antibiotic resistance index was calculated. Soil amendment with chicken litter significantly increased the number of antibiotic-resistant E. coli in the soil. Among the 126 E. coli isolates purified from all the samples, 76% showed resistance to at least one antibiotic, of which 54.2% were multidrug-resistant (MDR). The highest percentage resistance was to tetracycline (78.1%), with the least percentage resistance (3.1%) to imipenem, tigecycline, and gentamicin. The isolates also showed resistance to chloramphenicol (63.5%), ampicillin (58.3%), trimethoprim-sulfamethoxazole (39.6%), cefotaxime (30.2%), ceftriaxone (26.0%), cephalexin (20.8%), cefepime (11.5%), amoxicillin-clavulanic acid (11.5%), cefoxitin (10.4%), Nalidixic acid (9.4%), amikacin (6.3%), and ciprofloxacin (4.2%). Of the 54.2% (52/96) MDR, the highest number was isolated from the litter-amended soil (61.5%) and the least isolates from soil samples collected before litter application (1.9%). The relatively higher mean MAR index of the litter-amended soil (0.14), compared to the soil before the amendment (0.04), suggests soil pollution with antibiotic-resistant E. coli from sources of high antibiotic use. E. coli could only be detected in the soil up to 42 days following manure application, making it a suitable short-term indicator of antibiotic resistance contamination. Notwithstanding its relatively short detectability/survival, the application of chicken litter appeared to transfer antibiotic-resistant E. coli to the soil, enhancing the soil resistome and highlighting the consequences of such agricultural practices on public health.https://www.frontiersin.org/articles/10.3389/fenvs.2021.751732/fullE colimultidrug-resistancechicken litterlitter-amended soilunamended soilenvironment |
| spellingShingle | Dorcas Oladayo Fatoba Daniel Gyamfi Amoako Daniel Gyamfi Amoako Akebe Luther King Abia Sabiha Yusuf Essack Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil Frontiers in Environmental Science E coli multidrug-resistance chicken litter litter-amended soil unamended soil environment |
| title | Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil |
| title_full | Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil |
| title_fullStr | Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil |
| title_full_unstemmed | Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil |
| title_short | Transmission of Antibiotic-Resistant Escherichia coli from Chicken Litter to Agricultural Soil |
| title_sort | transmission of antibiotic resistant escherichia coli from chicken litter to agricultural soil |
| topic | E coli multidrug-resistance chicken litter litter-amended soil unamended soil environment |
| url | https://www.frontiersin.org/articles/10.3389/fenvs.2021.751732/full |
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