Assessment of carbapenem resistance and carbapenemase genes in wastewater from cattle slaughterhouses: Implications for environmental antibiotic resistance surveillance
Öz
The objectives of the study were to determine the prevalence of carbapenem-resistant Gram-negative bacteria and assess the potential risks associated with cattle slaughterhouse wastewater. A total of 270 wastewater samples were collected from 10 different cattle slaughterhouses for microbiological analysis. Conventional culture methods were employed, followed by disc diffusion, the Modified Carbapenem Inactivation Method (mCIM), and the Modified Hodge Test (MHT) to identify carbapenem resistance. The Vitek® 2 compact system was used for species identification and antibiotic susceptibility profiling. Conventional and quantitative PCR (qPCR) were performed to detect specific carbapenemase genes (blaKPC, blaNDM, and blaOXA-48), among the collected 17 (6.30%) carbapenem-resistant isolates, one Pseudomonas fluorescens (0.37%), one Aeromonas hydrophila (0.37%), and two Aeromonas sobria (0.74%) exhibited resistance to meropenem. Additionally, six P. fluorescens (2.22%) and two A. hydrophila (0.74%) isolates demonstrated intermediate resistance to meropenem. Furthermore, five carbapenem-resistant isolates were identified as Stenotrophomonas maltophilia (1.85%), known to be inherently resistant to most antibiotics. Ten different antibiotics were evaluated in the antibiotic resistance panel and all Aeromonas isolates were found to be resistant to cefazolin and one A. hydrophila was detected as multi-drug resistant. The revealed data indicates that slaughterhouse wastewater can serve as a reservoir for antibiotic-resistant opportunistic pathogens. However, it may not pose a substantial risk for the distribution of carbapenemases, thereby mitigating concerns related to potential public health and environmental hazards associated with this aspect of slaughterhouse operations. This study contributes to understanding of antibiotic resistance in livestock-related environments and underscores the importance of continued monitoring and surveillance.
Anahtar Kelimeler
Carbapenem resistance carbapenemase genes slaughterhouses wastewater
Etik Beyan
This research was conducted in accordance with all applicable ethical guidelines and regulations.
Destekleyen Kurum
We would like to thank The Scientific and Technological Research Council of Türkiye (TÜBİTAK) for the financial support of this study granted under number 217O398.
Proje Numarası
217O398
Teşekkür
The authors are grateful for the financial support provided by The Scientific and Technological Research Council of Türkiye (TUBİTAK) through grant number 217O398. This funding was instrumental in enabling us to conduct the research presented in the research article.
Kaynakça
- Al S, Hizlisoy H, Ertas Onmaz N, et al (2020): A molecular investigation of carbapenem resistant Enterobacteriaceae and blaKPC, blaNDM and blaOXA-48 genes in raw milk. Kafkas Univ Vet Fak Derg, 26, 391-396.
- Aminov RI (2011): Horizontal gene exchange in environmental microbiota. Front Microbiol, 2, 158.
- Aurilio C, Sansone P, Barbarisi M, et al (2022): Mechanisms of action of carbapenem resistance. Antibiotics, 11, 421.
- Bauer AW, Kirby MM, Sherris JC, et al (1966): Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol, 45, 493-496.
- Buschhardt T, Günther T, Skjerdal T, et al (2021): A one health glossary to support communication and information exchange between the human health, animal health and food safety sectors. One Health, 13, 100263.
- Centers for Disease Control and Prevention (CDC) (2020): Laboratory protocol for detection of carbapenem-resistant or carbapenemase-producing, Klebsiella spp. or E. coli from rectal swabs. https://www.cdc.gov/HAI/pdfs/ labSettings/Klebsiella_or_Ecoli.pdf. (Accessed May 29, 2020).
- Chabou S, Leulmi H, Davoust B, et al (2018): Prevalence of extended-spectrum β-lactamase-and carbapenemase-encoding genes in poultry faeces from Algeria and Marseille, France. J Glob Antimicrob Resist, 13, 28-32.
- Chaw PS, Höpner J, Mikolajczyk R (2018): The knowledge, attitude and practice of health practitioners towards antibiotic prescribing and resistance in developing countries-A systematic review. J Clin Pharm Ther, 43, 606-613.
- Clinical and Laboratory Standards Institute (CLSI) (2014): Performance Standards for Antimicrobial Susceptibility Testing. 24th ed. CLSI standard M100-S24. Wayne, PA, USA.
- Clinical and Laboratory Standards Institute (CLSI) (2018): Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI standard M100-S28. Wayne, PA, USA.
- European Medicines Agency (EMA) (2019): Categorisation of antibiotics in the European Union. www.ema.europa.eu/en/documents/report/categorisation-antibiotics-european-union-answer-request-european-commission-updating-scientific-advice-impact-public-health-and-animal-health-use-antibiotics-animals_en.pdf. (Accessed Jan 17, 2024).
- Facciola A, Virga A, Gioffre ME, et al (2021): Evaluation of antibiotic resistance in bacterial strains isolated from sewage of slaughterhouses located in Sicily (Italy). Int J Environ Res Public Health, 18, 9611.
- Fouz N, Pangesti KN, Yasir M, et al (2020): The contribution of wastewater to the transmission of antimicrobial resistance in the environment: implications of mass gathering settings. Trop Med Infect Dis, 5, 33.
- Halat HD, Moubareck AC (2020): The current burden of carbapenemases: Review of significant properties and dissemination among gram-negative bacteria. Antibiotics, 9, 186.
- Hilt EE, Fitzwater SP, Ward K, et al (2020): Carbapenem Resistant Aeromonas hydrophila Carrying blaCphA7 Isolated from Two Solid Organ Transplant Patients. Front Cell Infect Microbiol, 10, 563482.
- Karampatakis T, Antachopoulos C, Tsakris A, et al (2018): Molecular epidemiology of carbapenem-resistant Pseudomonas aeruginosa in an endemic area: comparison with global data. Eur J Clin Microbiol Infect Dis; 37, 1211-1220.
- Larsson DJ, Flach CF (2022): Antibiotic resistance in the environment. Nat Rev Microbiol, 20, 257-269.
- Mann EE, Wozniak DJ (2012): Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev, 36, 893-916.
- Nordmann P, Poirel L (2019): Epidemiology and diagnostics of carbapenem resistance in gram-negative bacteria. Clin Infect Dis, 69, 521-528.
- Papp-Wallace KM, Endimiani A, Taracila MA, et al (2011): Carbapenems: past, present, and future. Antimicrob Agents Chemother, 55, 4943-4960.
- Partridge SR, Kwong SM, Firth N, et al (2018): Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev, 31, e00088-17.
- Pellegrini C, Mercuri PS, Celenza G, et al (2009): Identification of blaIMP-22 in Pseudomonas spp. in urban wastewater and nosocomial environments: biochemical characterization of a new IMP metallo-enzyme variant and its genetic location. J Antimicrob Chemother, 63, 901-908.
- Poirel L, Berçot B, Millemann Y, et al (2012): Carbapenemase-producing Acinetobacter spp. in cattle, France. Emerg Infect Dis, 18, 523e5.
- Poirel L, Walsh TR, Cuvillier V, et al (2011): Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis, 70, 119-123.
- Salam MA, Al-Amin MY, Salam A, et al (2023): Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Healthcare, 11, 1946.
- Subirats J, Royo E, Balcazar JL, et al (2017): Real-time PCR assays for the detection and quantification of carbapenemase genes (blaKPC, blaNDM, and blaOXA-48) in environmental samples. Environ Sci Pollut Res Int, 24, 6710-6714.
- Sun Y, Zhao Y, Xu W, et al (2021): Taxonomy, virulence determinants and antimicrobial susceptibility of Aeromonas spp. isolated from bacteremia in southeastern China. Antimicrob Resist Infect Control, 10, 1-9.
- The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2020): Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0. http://www.eucast.org. (Accessed Jun 24, 2020).
- Velazquez-Meza ME, Galarde-Lopez M, Carrillo-Quiroz B, et al (2022): Antimicrobial resistance: one health approach. Vet World, 15, 743.
- Wong MHY, chi Chan EW, Chen S (2015): Isolation of carbapenem-resistant Pseudomonas spp. from food. J Glob Antimicrob Resist, 3, 109-114.
Öz
Proje Numarası
217O398
Kaynakça
- Al S, Hizlisoy H, Ertas Onmaz N, et al (2020): A molecular investigation of carbapenem resistant Enterobacteriaceae and blaKPC, blaNDM and blaOXA-48 genes in raw milk. Kafkas Univ Vet Fak Derg, 26, 391-396.
- Aminov RI (2011): Horizontal gene exchange in environmental microbiota. Front Microbiol, 2, 158.
- Aurilio C, Sansone P, Barbarisi M, et al (2022): Mechanisms of action of carbapenem resistance. Antibiotics, 11, 421.
- Bauer AW, Kirby MM, Sherris JC, et al (1966): Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol, 45, 493-496.
- Buschhardt T, Günther T, Skjerdal T, et al (2021): A one health glossary to support communication and information exchange between the human health, animal health and food safety sectors. One Health, 13, 100263.
- Centers for Disease Control and Prevention (CDC) (2020): Laboratory protocol for detection of carbapenem-resistant or carbapenemase-producing, Klebsiella spp. or E. coli from rectal swabs. https://www.cdc.gov/HAI/pdfs/ labSettings/Klebsiella_or_Ecoli.pdf. (Accessed May 29, 2020).
- Chabou S, Leulmi H, Davoust B, et al (2018): Prevalence of extended-spectrum β-lactamase-and carbapenemase-encoding genes in poultry faeces from Algeria and Marseille, France. J Glob Antimicrob Resist, 13, 28-32.
- Chaw PS, Höpner J, Mikolajczyk R (2018): The knowledge, attitude and practice of health practitioners towards antibiotic prescribing and resistance in developing countries-A systematic review. J Clin Pharm Ther, 43, 606-613.
- Clinical and Laboratory Standards Institute (CLSI) (2014): Performance Standards for Antimicrobial Susceptibility Testing. 24th ed. CLSI standard M100-S24. Wayne, PA, USA.
- Clinical and Laboratory Standards Institute (CLSI) (2018): Performance Standards for Antimicrobial Susceptibility Testing. 28th ed. CLSI standard M100-S28. Wayne, PA, USA.
- European Medicines Agency (EMA) (2019): Categorisation of antibiotics in the European Union. www.ema.europa.eu/en/documents/report/categorisation-antibiotics-european-union-answer-request-european-commission-updating-scientific-advice-impact-public-health-and-animal-health-use-antibiotics-animals_en.pdf. (Accessed Jan 17, 2024).
- Facciola A, Virga A, Gioffre ME, et al (2021): Evaluation of antibiotic resistance in bacterial strains isolated from sewage of slaughterhouses located in Sicily (Italy). Int J Environ Res Public Health, 18, 9611.
- Fouz N, Pangesti KN, Yasir M, et al (2020): The contribution of wastewater to the transmission of antimicrobial resistance in the environment: implications of mass gathering settings. Trop Med Infect Dis, 5, 33.
- Halat HD, Moubareck AC (2020): The current burden of carbapenemases: Review of significant properties and dissemination among gram-negative bacteria. Antibiotics, 9, 186.
- Hilt EE, Fitzwater SP, Ward K, et al (2020): Carbapenem Resistant Aeromonas hydrophila Carrying blaCphA7 Isolated from Two Solid Organ Transplant Patients. Front Cell Infect Microbiol, 10, 563482.
- Karampatakis T, Antachopoulos C, Tsakris A, et al (2018): Molecular epidemiology of carbapenem-resistant Pseudomonas aeruginosa in an endemic area: comparison with global data. Eur J Clin Microbiol Infect Dis; 37, 1211-1220.
- Larsson DJ, Flach CF (2022): Antibiotic resistance in the environment. Nat Rev Microbiol, 20, 257-269.
- Mann EE, Wozniak DJ (2012): Pseudomonas biofilm matrix composition and niche biology. FEMS Microbiol Rev, 36, 893-916.
- Nordmann P, Poirel L (2019): Epidemiology and diagnostics of carbapenem resistance in gram-negative bacteria. Clin Infect Dis, 69, 521-528.
- Papp-Wallace KM, Endimiani A, Taracila MA, et al (2011): Carbapenems: past, present, and future. Antimicrob Agents Chemother, 55, 4943-4960.
- Partridge SR, Kwong SM, Firth N, et al (2018): Mobile genetic elements associated with antimicrobial resistance. Clin Microbiol Rev, 31, e00088-17.
- Pellegrini C, Mercuri PS, Celenza G, et al (2009): Identification of blaIMP-22 in Pseudomonas spp. in urban wastewater and nosocomial environments: biochemical characterization of a new IMP metallo-enzyme variant and its genetic location. J Antimicrob Chemother, 63, 901-908.
- Poirel L, Berçot B, Millemann Y, et al (2012): Carbapenemase-producing Acinetobacter spp. in cattle, France. Emerg Infect Dis, 18, 523e5.
- Poirel L, Walsh TR, Cuvillier V, et al (2011): Multiplex PCR for detection of acquired carbapenemase genes. Diagn Microbiol Infect Dis, 70, 119-123.
- Salam MA, Al-Amin MY, Salam A, et al (2023): Antimicrobial Resistance: A Growing Serious Threat for Global Public Health. Healthcare, 11, 1946.
- Subirats J, Royo E, Balcazar JL, et al (2017): Real-time PCR assays for the detection and quantification of carbapenemase genes (blaKPC, blaNDM, and blaOXA-48) in environmental samples. Environ Sci Pollut Res Int, 24, 6710-6714.
- Sun Y, Zhao Y, Xu W, et al (2021): Taxonomy, virulence determinants and antimicrobial susceptibility of Aeromonas spp. isolated from bacteremia in southeastern China. Antimicrob Resist Infect Control, 10, 1-9.
- The European Committee on Antimicrobial Susceptibility Testing (EUCAST) (2020): Breakpoint tables for interpretation of MICs and zone diameters. Version 10.0. http://www.eucast.org. (Accessed Jun 24, 2020).
- Velazquez-Meza ME, Galarde-Lopez M, Carrillo-Quiroz B, et al (2022): Antimicrobial resistance: one health approach. Vet World, 15, 743.
- Wong MHY, chi Chan EW, Chen S (2015): Isolation of carbapenem-resistant Pseudomonas spp. from food. J Glob Antimicrob Resist, 3, 109-114.
Ayrıntılar
| Birincil Dil | İngilizce |
|---|---|
| Konular | Veteriner Gıda Hijyeni ve Teknolojisi |
| Bölüm | Araştırma Makalesi |
| Yazarlar | |
| Proje Numarası | 217O398 |
| Yayımlanma Tarihi | |
| Gönderilme Tarihi | 7 Şubat 2024 |
| Kabul Tarihi | 31 Temmuz 2024 |
| Yayımlandığı Sayı | Yıl 2025Cilt: 72 Sayı: 1 |
