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

İlyas Kuşcu; Saffet Alper Ünlükal; Muammer Göncüoğlu

doi:10.59124/guhes.1430980

EN

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

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

Details

Primary Language

English

Subjects

Clinical Sciences (Other)

Journal Section

Research Article

Authors

İlyas Kuşcu ^*
0000-0003-3667-3066
Türkiye

Saffet Alper Ünlükal
0000-0003-1105-2140
Türkiye

Muammer Göncüoğlu
0000-0001-7245-1941
Türkiye

Publication Date

April 30, 2024

Submission Date

February 5, 2024

Acceptance Date

April 4, 2024

Published in Issue

Year 2024 Volume: 6 Number: 1

DOI

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

IZ

https://izlik.org/JA39BH35GP

APA

Kuşcu, İ., Ünlükal, S. A., & Göncüoğlu, M. (2024). Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae. Journal of Gazi University Health Sciences Institute, 6(1), 18-28. https://doi.org/10.59124/guhes.1430980

AMA

1.Kuşcu İ, Ünlükal SA, Göncüoğlu M. Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae. GUHES. 2024;6(1):18-28. doi:10.59124/guhes.1430980

Chicago

Kuşcu, İlyas, Saffet Alper Ünlükal, and Muammer Göncüoğlu. 2024. “Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae”. Journal of Gazi University Health Sciences Institute 6 (1): 18-28. https://doi.org/10.59124/guhes.1430980.

EndNote

Kuşcu İ, Ünlükal SA, Göncüoğlu M (April 1, 2024) Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae. Journal of Gazi University Health Sciences Institute 6 1 18–28.

IEEE

[1]İ. Kuşcu, S. A. Ünlükal, and M. Göncüoğlu, “Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae”, GUHES, vol. 6, no. 1, pp. 18–28, Apr. 2024, doi: 10.59124/guhes.1430980.

ISNAD

Kuşcu, İlyas - Ünlükal, Saffet Alper - Göncüoğlu, Muammer. “Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae”. Journal of Gazi University Health Sciences Institute 6/1 (April 1, 2024): 18-28. https://doi.org/10.59124/guhes.1430980.

JAMA

1.Kuşcu İ, Ünlükal SA, Göncüoğlu M. Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae. GUHES. 2024;6:18–28.

MLA

Kuşcu, İlyas, et al. “Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae”. Journal of Gazi University Health Sciences Institute, vol. 6, no. 1, Apr. 2024, pp. 18-28, doi:10.59124/guhes.1430980.

Vancouver

1.İlyas Kuşcu, Saffet Alper Ünlükal, Muammer Göncüoğlu. Investigation of the Resistance of Some Disinfectant Active Substances in ESBL-Producing Enterobacteriaceae. GUHES. 2024 Apr. 1;6(1):18-2. doi:10.59124/guhes.1430980

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

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