Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae

Year 2024, Volume: 6 Issue: 1, 18 - 28, 30.04.2024

İlyas Kuşcu Saffet Alper Ünlükal Muammer Göncüoğlu

https://doi.org/10.59124/guhes.1430980

Abstract

In this study, a total of 200 samples, including 100 neck skin and 100 cecum samples, were collected and analyzed from various poultry slaughterhouses on different sampling days. ESBL-producing Enterobacteriaceae were isolated and ESBL production was confirmed phenotypically by combined disk diffusion and E-test gradient strips. While ESBL production was confirmed in 10 (10%) of 100 neck skin samples, no significant ESBL production could be confirmed in 100 cecal samples. The broth microdilution method of Clinical and Laboratory Standards Institute (CLSI) was used to determine the resistance profiles against benzalkonium chloride (BC), cetylpyridinium chloride (CPC), N-alkyl dimethyl benzyl ammonium chloride (ADBAC) and potassium peroxymonosulfate (PPMS) disinfectants in 10 neck skin isolates with confirmed ESBL production. In the study, it has been determined that MIC50 and MIC90 values were respectively ADBAC (8 and 16 mg/L), BC (16 and 32 mg/L), CPC (16, and 32 mg/L), PPMS (≥ 1024 mg/L). The impacts of Enterobacteriaceae strains on food safety and public health are significant; Disinfectant resistance can lead to increased transmission of antibiotic-resistant bacteria, leading to serious infections in humans that are difficult to treat. For that reason, it is of great importance to develop effective control methods, including appropriate disinfectant use, hand hygiene and appropriate isolation measures, to prevent the spread of disinfectant resistant Enterobacteriaceae strains in food production systems.

Keywords

Public health, disinfectant resistance, Enterobacteriaceae ESBL resistance

References

• Akyüz, H. Ö., Aytekin, İ. (2022). Covid-19 Sürecinde Koruyucu Sağlık ve Hijyen Ürünlerinin Satışı ve Tüketimi Üzerine Bir İnceleme. Medical Research Reports, 5(1), 27-39. https://doi.org/10.55517/mrr.1062587
• Anes, J., ccusker, M. P., Fanning, S., Martins, M. (2015). The ins and outs of RND efflux pumps in Escherichia coli. Frontiers in Microbiology, 6, 587. https://doi.org/10.3389/fmicb.2015.00587
• Bertrand, S., Weill, F. X., Cloeckaert, A., Vrints, M., Mairiaux, E., Praud, K., ... & Collard, J. M. (2006). Clonal emergence of extended-spectrum β-lactamase (CTX-M-2)-producing Salmonella enterica serovar Virchow isolates with reduced susceptibilities to ciprofloxacin among poultry and humans in Belgium and France (2000 to 2003). Journal of Clinical Microbiology, 44(8), 2897-2903. https://doi.org/10.1128/jcm.02549-05
• Boutarfi. Z., Rebiahi, S. A., Morghad, T., Pulido, R. P., Burgos, M. J. G., Mahdi, F., Lucas, R., Galvez, A. (2019). Biocide tolerance and antibiotic resistance of Enterobacter spp. isolated from an Algerian hospital environment. Journal of Global Antimicrobial Resistance, 18, 291-297. https://doi.org/10.1016/j.jgar.2019.04.005
• Boyce, J. M. (2023). Quaternary ammonium disinfectants and antiseptics: tolerance, resistance and potential impact on antibiotic resistance. Antimicrobial Resistance & Infection Control, 12-32. https://doi.org/10.1186/s13756-023-01241-z
• Breijyeh, Z., Jubeh, B., & Karaman, R. (2020). Resistance of Gram Negative Bacteria to Current Antibacterial Agents and Approaches to Resolve It. Molecules, 25(6), 1340. https://doi.org/10.3390/molecules25061340
• Cai, L., Wang, H., Liang, L., Wang, G., Xu, X., & Wang, H. (2018). Response of Formed-Biofilm of Enterobacter cloacae, Klebsiella oxytoca, and Citrobacter freundii to Chlorite-Based Disinfectants. Food Science, 83(5), 1326-1332. https://doi.org/10.1111/1750-3841.14149
• Centers for Disesase Control and Prevention (CDC) (2019). ESBL-producing Enterobacterales in Healthcare setting. Retrieved from: https://www.cdc.gov/hai/organisms/ESBL.html
• Chapuis, A., Amoureux, L., Bador, J., Gavalas, A., Siebor, E., Chrétien, M., Caillot, D., Janin, M., Curraize, C., & Neuwirth, C. (2016). Outbreak of Extended-Spectrum Beta-Lactamase producing Enterobacter cloacae with high MICs of Quaternary Ammonium Compounds in a Hematology Ward Associated with contaminated sinks. Frontiers in Microbiology, 7, 1070. https://doi.org/10.3389/fmicb.2016.01070
• Chmielewski, R. A. N., & Frank, J. F. (2003). Biofilm formation and control in food processing facilities. Comprehensive Reviews in Food Science and Food Safety, 2(1), 22-32. https://doi.org/10.1111/j.1541-4337.2003.tb00012.x
• Clinical and Laboratory Standards Institute (CLSI). (2018). CLSI methods for dilution antimicrobial susceptibility tests for bacteria that grow aerobically. CLSI standard M07. Wayne, PA: Clinical and Laboratory Standards Institute.
• Damiano, P., Salema, E. J., & Silago, V. (2021). The susceptibility of multidrug resistant and biofilm forming Klebsiella pneumoniae and Escherichia coli to antiseptic agents used for preoperative skin preparations at zonal referral hospital in Mwanza, Tanzania. Malawi Medical Journal, 33(1), 59-64. https://www.mmj.mw/?p=11890
• Denton, M. (2007). Enterobacteriaceae. International Journal of Antimicrobial Agents, 29, 9-22. https://doi.org/10.1016/S0924-8579(07)72174-X
• Deus, D., Krischek, C., Pfeifer, Y., Sharifi, A. R., Fiegen, U., Reich, F., ... & Kehrenberg, C. (2017). Comparative analysis of the susceptibility to biocides and heavy metals of extended-spectrum β-lactamase-producing Escherichia coli isolates of human and avian origin, Germany. Diagnostic Microbiology and Infectious Disease, 88(1), 88-92. https://doi.org/10.1016/j.diagmicrobio.2017.01.023
• Dumaru, R., Baral, R., & Shrestha, L. B. (2019). Study of biofilm formation and antibiotic resistance pattern of gram-negative Bacilli among the clinical isolates at BPKIHS, Dharan. BMC Research Notes, 12, 1-6. https://doi.org/10.1186/s13104-019-4084-8
• El Harrif-Heraud, Z., Arpin, C., Benliman, S., & Quentin, C. (1997). Molecular epidemiology of a nosocomial outbreak due to SHV-4-producing strains of Citrobacter diversus. Journal of Clinical Microbiology, 35(10), 2561-2567. https://doi.org/10.1128/jcm.35.10.2561-2567.1997
• Halk Sağlığı Genel Müdürlüğü. (2023). Retrieved from: http://cbs.cevresaglik.gov.tr/cevresaglik/Biyosidal/Dezenfektan.aspx
• Hasman, H., Mevius, D., Veldman, K., Olesen, I., & Aarestrup, F. M. (2005). β-Lactamases among extended-spectrum β-lactamase (ESBL)-resistant Salmonella from poultry, poultry products and human patients in The Netherlands. Journal of Antimicrobial Chemotherapy, 56(1), 115-121. https://doi.org/10.1093/jac/dki190
• Hibbert-Rogers, L. C., Heritage, J., Gascoyne-Binzi, D. M., Hawkey, P. M., Todd, N., Lewis, I. J., & Bailey, C. (1995). Molecular epidemiology of ceftazidime resistant Enterobacteriaceae from patients on a paediatric oncology ward. Journal of Antimicrobial Chemotherapy, 36(1), 65-82. https://doi.org/10.1093/jac/36.1.65
• Hrovat, K., Zupančič, J. Č., Seme, K., & Avguštin, J. (2023). QAC Resistance Genes in ESBL-Producing E. coli Isolated from Patients with Lower Respiratory Tract Infections in the Central Slovenia Region: A 21-Year Survey. Tropical Medicine and Infectious Disease, 8(5), 273. https://doi.org/10.3390/tropicalmed8050273
• Laconi, A., Tolosi, R., Apostolakos, I., & Piccirillo, A. (2023). Biofilm Formation Ability of ESBL/pAmpC-Producing Escherichia coli Isolated from the Broiler Production Pyramid. Antibiotics, 12(1), 155. https://doi.org/10.3390/antibiotics12010155
• Liebana, E., Batchelor, M., Hopkins, K. L., Clifton-Hadley, F. A., Teale, C. J., Foster, A., ... & Davies, R. H. (2006). Longitudinal farm study of extended-spectrum β-lactamase-mediated resistance. Journal of Clinical Microbiology, 44(5), 1630-1634. https://doi.org/10.1128/jcm.44.5.1630-1634.2006
• Morrissey, I., Oggioni, M. R., Knight, D., Curiao, T., Coque, T., Kalkanci, A., & Martinez, J. L. (2014). Evaluation of epidemiological cut-off values indicates that biocide resistant subpopulations are uncommon in natural isolates of clinically-relevant microorganisms. PloS One, 9(1), e86669. https://doi.org/10.1371/journal.pone.0086669
• Murugesan, S., McCarthy, C. M., Michelle, K. S., Linzhi, W., Dillon, J. R., Joseph, E. R., & Aaron, P. W. (2022). Biofilm Formation and Antimicrobial Susceptibility of E. coli Associated With Colibacillosis Outbreaks in Broiler Chickens From Saskatchewan. Frontiers in Microbiology, 13, 841516. https://doi.org/10.3389/fmicb.2022.841516
• Navon-Venezia, S., Kondratyeva, K., & Carattoli, A. (2017). Klebsiella pneumoniae: a major worldwide source and shuttle for antibiotic resistance. FEMS Microbiology Reviews, 41, 252–275. https://doi.org/10.1093/femsre/fux013
• Nguyen, T. H. T., Nguyen, H. D., Le, M. H., Nguyen, T. T. H., Nguyen, T. D., Nguyen, D. L., ... & Pham, H. N. (2023). Efflux Pump Inhibitors in Controlling Antibiotic Resistance: Outlook under a Heavy Metal Contamination Context. Molecules, 28(7), 2912. https://doi.org/10.3390/molecules28072912
• Palucha, A., Mikiewicz, B., & Gniadkowski, M. (1999). Mechanisms of resistance - Diversification of Escherichia coli Expressing an SHV-Type Extended-Spectrum β-Lactamase (ESBL) during a Hospital Outbreak: Emergence of an ESBL-Hyperproducing Strain. Antimicrobial Agents and Chemotherapy, 43(2), 393-396. https://doi.org/10.1128/aac.43.2.393
• Riano, I., Moreno, M. A., Teshager, T., Saenz, Y., Domínguez, L., & Torres, C. (2006). Detection and characterization of extended-spectrum β-lactamases in Salmonella enterica strains of healthy food animals in Spain. Journal of Antimicrobial Chemotherapy, 58(4), 844-847. https://doi.org/10.1093/jac/dkl337
• Rolbiecki, D., Korzeniewska, E., Czatzkowska, M., & Harnisz, M. (2022). The Impact of Chlorine Disinfection of Hospital Wastewater on Clonal Similarity and ESBL-Production in Selected Bacteria of the Family Enterobacteriaceae. International Journal of Environmental Research and Public Health, 19(21), 13868. https://doi.org/10.3390/ijerph192113868
• Shaikh, S., Fatima, J., Shakil, S., Rizvi, S., & Kamal, Ma. (2015). Antibiotic resistance and extended spectrum beta-lactamases: Types, epidemiology and treatment. Journal of Saudi Biological Sciences, 22, 90-101. https://doi.org/10.1016/j.sjbs.2014.08.002
• Sun, Y., Hu, X., Guo, D., Shi, C., Zhang, C., Peng, X., ... & Xia, X. (2019). Disinfectant Resistance Profiles and Biofilm Formation Capacity of Escherichia coli Isolated from Retail Chicken. Microbial Drug Resistance, 25(5), 703-711. https://doi.org/10.1089/mdr.2018.0175
• The European Committee on Antimicrobial Susceptibility Testing (EUCAST). (2017). EUCAST guidelines for detection of resistance mechanisms and specific resistances of clinical and/or epidemiological importance. Retrieved from https://www.eucast.org/resistance_mechanisms
• Tong, C., Hu, H., Chen, G., Li, Z., Li, A., & Zhang, J. (2021). Disinfectant resistance in bacteria: Mechanisms, spread, and resolution strategies. Environmental Research, 195, 10897. https://doi.org/10.1016/j.envres.2021.110897
• Vahaboglu, H., Dodanli, S., Eroglu, C., Oztürk, R., Soyletir, G., Yildirim, I., & Avkan, V. (1996). Characterization of multiple-antibiotic-resistant Salmonella typhimurium strains: molecular epidemiology of PER-1-producing isolates and evidence for nosocomial plasmid exchange by a clone. Journal of Clinical Microbiology, 34(12), 2942-2946. https://doi.org/10.1128/jcm.34.12.2942-2946.1996
• Valverde, A., Coque, T. M., Sánchez-Moreno, M. P., Rollán, A., Baquero, F., & Cantón, R. (2004). Dramatic increase in prevalence of fecal carriage of extended-spectrum β-lactamase-producing Enterobacteriaceae during nonoutbreak situations in Spain. Journal of Clinical Microbiology, 42(10), 4769-4775. https://doi.org/10.1128/jcm.42.10.4769-4775.2004
• Venezia, R. A., Scarano, F. J., Preston, K. E., Steele, L. M., Root, T. P., Limberger, R., ... & Kacica, M. A. (1995). Molecular epidemiology of an SHV-5 extended-spectrum β-lactamase in Enterobacteriaceae isolated from infants in a neonatal intensive care unit. Clinical Infectious Diseases, 21(4), 915-923. https://doi.org/10.1093/clinids/21.4.915
• World Health Organization (WHO). (2023). Foodborne diseases. Retrieved from https://www.who.int/health-topics/foodborne-diseases#tab=tab_1
• Wu, G., Yang, Q., Long, M., Guo, L., Li, B., Meng, Y., Zhang, A., Wang, H., Liu, S., & Zou, L. (2015). Evaluation of agar dilution and broth microdilution methods to determine the disinfectant susceptibility. The Journal of Antibiotics, 68(11), 661-665. https://doi.org/10.1038/ja.2015.51
• Yılmaz, E. S., & Güvensen, N. C. (2016). In vitro biofilm formation in ESBL producing Escherichia coli isolates from cage birds. Asian Pacific Journal of Tropical Medicine, 9(11), 1069-1074. https://doi.org/10.1016/j.apjtm.2016.10.003
• Zhang, A., He, X., Meng, Y., Guo, L., Long, M., Yu, H., Li, B., Fan, L., Liu, S., Wang, H., & Zou, L. (2016). Antibiotic and Disinfectant Resistance of Escherichia coli Isolated from Retail Meats in Sichuan, China. Journal of Microbial Drug Resistance, 22, 80-87. https://doi.org/10.1089/mdr.2015.0061