Detection and prevalence of extended spectrum β-lactamases production among Enterobacteriaceae isolated from urinary tract infections
Keywords:
antimicrobial susceptibility; urinary tract infections (UTIs); Enterobacteriaceae; extended-spectrum β-lactamases (ESBL) – producing; multi-drug resistance
Abstract
Urinary tract infections (UTIs) by extended-spectrum β-lactamase producing Enterobacteriaceae (ESBL-E) have become an important public health problem with a substantial economic burden, as they lead to more complicated infections, longer duration of treatment, and increases in patient mortality. A total of 1267 urine samples were collected from patients during the period of 2018 to 2020. The isolates were identified based on colony morphology and biochemical tests. Antimicrobial susceptibility testing was done by modified Kirby Bauer disc diffusion method. Resistant isolates to third generation cephalosporins were tested for ESBL production by double-disk synergy test (DDST), DDST methods on MH agar plates supplemented with cloxacillin and by confirmatory double disk test (DDT). 400 strains causing UTIs were identified and classified as members of Enterobacteriaceae. The results of antimicrobial susceptibility tests showed that 68.5% (274/400) of the Enterobacteriaceae isolates were multi-drug resistant (MDR) strains. The overall prevalence of ESBL-E was 59.5% (238/400). The highest frequencies of ESBL-E were observed in internal medicine devices (68/400) and the highest ESBL production was observed in E. coli (85/238). The ESBL producing isolates were significantly resistant to penicillins and cephalosporins compared to non-ESBL producers. However, those ESBL-E strains were sensitive to imipenem (80.2%) and nitrofurantoin (87.8%). High levels of MDR strains and ESBL-E in our study highlights the need for applying specific infection control measures, and accordingly we urge physicians to opt for specific strategies for regular surveillance of uropathogenic bacteria.References
Abujnah, A. A., Zorgani, A., Sabri, M. A. M., El-Mohammady, H., Khalek, R. A., & Ghenghesh, K. S. (2015). Multidrug resistance and extended-spectrum β-lactamases genes among Escherichia coli from patients with urinary tract infections in Northwestern Libya. Libyan Journal of Medicine, 10, 26412.
Alasmary, M. Y. (2021). Antimicrobial resistance patterns and ESBL of uropathogens isolated from adult females in Najran region of Saudi Arabia. Clinical Practice, 11, 650–658.
Alibi, S., Ferjani, A., & Boukadida, J. (2015). Molecular characterization of extended spectrum beta-lactamases produced by Klebsiella pneumoniae clinical strains from a Tunisian Hospital. Médecine et Maladies Infectieuses, 45(4), 139–143.
Al-Mayahie, S., & Al Kuriashy, J. J. (2016). Distribution of ESBLs among Escherichia coli isolates from outpatients with recurrent UTIs and their antimicrobial resistance. The Journal of Infection in Developing Countries, 10(6), 575–583.
Benyagoub, E., Alkhudhairy, M. K., Benchaib, S. M., Zaalan, A., Mekhfi, Y., Teyebi, N., Razni, D., & Bendada, F. (2021). Isolation frequency of uropathogenic strains and search for ESBL producing Enterobacteriaceae isolated from patients with UTI in Bechar (Algeria). Anti-Infective Agents, 19(3), 303–316.
Critchley, I. A., Cotroneo, N., Pucci, M. J., & Mendes, R. (2019). The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017. PloS One, 14(12), 0220265.
Dash, N. R., Albataineh, M. T., Alhourani, N., Khoudeir, A. M., Ghanim, M., Wasim, M., & Mahmoud, I. (2018). Community-acquired urinary tract infections due to extended-spectrum β-lactamase-producing organisms in United Arab Emirates. Travel Medicine and Infectious Disease, 22, 46–50.
De Angelis, G., Del Giacomo, P., Posteraro, B., Sanguinetti, M., & Tumbarello, M. (2020). Molecular mechanisms, epidemiology and clinical importance of β-lactam resistance in Enterobacteriaceae. International Journal of Molecular Sciences, 21, 5090.
El bouamri, M. C., Arsalane, L., Zerouali, K., Katfy, K., El kamouni, Y., Zouhair, S. (2015). Molecular characterization of extended spectrum β-lactamase-producing Escherichia coli in a university hospital in Morocco, North Africa. African Journal of Urology, 21, 161–166.
Gharavi, M. J., Zarei, J., Roshani-Asl, P., Yazdanyar, Z., Sharif, M., & Rashidi, N. (2021). Comprehensive study of antimicrobial susceptibility pattern and extended spectrum beta-lactamase (ESBL) prevalence in bacteria isolated from urine samples. Scientific Reports, 11(1), 578.
Halabi, M. K., Lahlou, F. A., Diawara, I., Adouzi, Y. E., Marnaoui, R., Benmessaoud, R., & Smyej, I. (2021). Antibiotic resistance pattern of extended spectrum beta lactamase producing Escherichia coli isolated from patients with urinary tract infection in Morocco. Frontiers in Cellular and Infection Microbiology, 2021, 720701.
Hantalo, A. H., Taassaw, K. H., Solomon, F. B., & Woldeamanuel, Y. (2020). Isolation and antibiotic susceptibility pattern of bacterial uropathogens and associated factors among adult people living with HIV/AIDS attending the HIV Center at Wolaita Sodo University Teaching Referral Hospital, South Ethiopia. HIV/AIDS: Research and Palliative Care, 12, 799–808.
Hassuna, N. A., Khairalla, A. S., Farahat, E. M., Hammad, A. M., & Abdel-Fattah, M. (2020). Molecular characterization of extended-spectrum β-lactamase producing E. coli recovered from community-acquired urinary tract infections in Upper Egypt. Scientific Reports, 10, 2772.
Jarlier, V., Nicolas, M. H., Fournier, G., & Philippon, A. (1988). Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns. Reviews of Infectious Diseases, 10, 867–878.
Kharrat, M., Chebbi, Y., Tanfous, F. B., Lakhal, A., Ladeb, S., Othmen, T. B., & Achour, W. (2018). Extended spectrum beta-lactamase-producing Enterobacteriaceae infections in hematopoietic stem cell transplant recipients: Epidemiology and molecular characterization. International Journal of Antimicrobial Agents, 52(6), 886–892.
Kunishima, H., Ishibashi, N., Wada, K., Oka, K., Takahashi, M., Yamasaki, Y., Aoyagi, T., Takemura, H., Kitagawa, M., & Kaku, M. (2019). The effect of gut microbiota and probiotic organisms on the properties of extended spectrum beta-lactamase producing and carbapenem resistant Enterobacteriaceae including growth, beta-lactamase activity and gene transmissibility. Journal of Infection and Chemotherapy, 25(11), 894–900.
Lin, S. P., Liu, M. F., Lin, C. F., & Shi, Z. Y. (2012). Phenotypic detection and polymerase chain reaction screening of extended-spectrum b-lactamases produced by Pseudomonas aeruginosa isolates. Journal of Microbiology, Immunology and Infection, 45(3), 200–207.
Magiorakos, A. P, Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B, Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (2012). Multidrug resistant, extensively drug-resistant and pan-drug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281.
Mazzariol, A., Bazaj, A., & Cornaglia, G. (2017). Multidrug-resistant Gram-negative bacteria causing urinary tract infections: A review. Journal of Chemotherapy, 29(suppl. 1), 2–9.
Mechai, A., Debabza, M., Fares, R., Metrouh, R., & Amra, A. (2020). Antibiotic susceptibility pattern and phenotypic characterization of extended-spectrum-beta-lactamase-producing Enterobacteriaceae isolated from various clinical samples. Environmental Engineering and Management Journal, 19(12), 2139–2146.
Mohammed, M. A., Alnour, T. M. S., Shakurfo, O. M., & Aburass, M. M. (2016). Prevalence and antimicrobial resistance pattern of bacterial strains isolated from patients with urinary tract infection in Messalata Central Hospital, Libya. Asian Pacific Journal of Tropical Medicine, 9(8), 771–776.
Muthupandian, S., Ramachandran, B., & Barabadic, H. (2018). The prevalence and drug resistance pattern of extended spectrum β-lactamases (ESBLs) producing Enterobacteriaceae in Africa. Microbial Pathogenesis, 114, 180–192.
Nabti, L. Z, Sahli, F., Radji, N., Mezaghcha, W., Semara, L., Aberkane, S., Lounnas, M., Solassol, J., Didelot, M. N., Jean-Pierre, H., Dumont, Y., & Godreuil, S. (2019). High prevalence of multidrug-resistant Escherichia coli in urine samples from inpatients and outpatients at a tertiary care hospital in Setif, Algeria. Microbial Drug Resistance, 25(3), 386–393.
Natoubi, S., Barguigua, A., Diawara, I., Timinouni, M., Rakib, K., Amghar, S., & Zerouali, K. (2020). Epidemiology of extended-spectrum β-lactamases and carbapenemases producing Enterobacteriaceae in Morocco. Journal of Contemporary Clinical Practice, 6(2), 75–85.
Rahal, K. (2005). Standardisation de l’antibiogramme en Médecine Humaine à l’échelle nationale selon les recommandations de l’OMS. 4th edition. Algeria.
Rania, Y. Shash, L., Elshimy, A. A., Soliman, M. Y., & Mosharafa, A. A. (2019). Molecular characterization of extended-spectrum β-lactamase Enterobacteriaceae isolated from Egyptian patients with community- and hospital-acquired urinary tract infection. American Journal of Tropical Medicine and Hygiene, 100(3), 522–528.
Raya, G. B., Dhoubhadel, B. G., Shrestha, D. P., Raya, S., Laghu, U., Shah, A., Raya, B. B., Kafle, R., Parry, C. M., & Ariyoshi, K. (2020). Multidrug-resistant and extended-spectrum beta-lactamase-producing uropathogens in children in Bhaktapur, Nepal. Tropical Medicine and Health, 48(1), 65.
Sbiti, M., Lahmadi, K., & Louzi, L. (2017). Profil épidémiologique des entérobactéries uropathogènes productrices de bêta-lactamases à spectre élargi. The Pan African Medical Journal, 28, 29.
Somily, A. M., Habib, H. A., Absar, M., Arshad, M., Manneh, K., Subaie, S. S. A., Hedaithy, M. A. A., Sayyed, S. B., Shakoor, Z., & Murray, T. F. (2014). ESBL-producing Escherichia coli and Klebsiella pneumoniae at a tertiary care hospital in Saudi Arabia. Journal of Infection in Developing Countries, 8(9), 1129–1136.
Tayh, G., Laham, N. A., Yahia, H. B., Sallem, R. B., Elottol, A. E. K. Y., & Slama, K. B. (2019). Extended-spectrum β-lactamases among Enterobacteriaceae isolated from urinary tract infections in Gaza Strip, Palestine. BioMed Research International, 2019, 4041801.
Tekele, S. G., Teklu, D. S., Tullu, K. D., Birru, S. K., & Legese, M. H. (2020). Extended-spectrum betalactamase and AmpC beta-lactamases producing gram negative bacilli isolated from clinical specimens at international clinical laboratories, Addis Ababa, Ethiopia. PLoS One, 15(11), e0241984.
Tooke, C. L., Hinchliffe, P., Bragginton, E. C., Colenso, C. K., Hirvonen, V. H. A., Takebayashi, Y., & Spencer, J. (2019). β-Lactamases and β-lactamase inhibitors in the 21st century. Journal of Molecular Biology, 431(18), 3472–3500.
Zenati, F., Barguigua, A., Nayme, K., Benbelaïd, F., Khadir, A., Bellahsene, C., Bendahou, M., Hafida, H., & Timinouni, M. (2019). Characterization of uropathogenic ESBL-producing Escherichia coli isolated from hospitalized patients in Western Algeria. Journal of Infection in Developing Countries, 13(4), 291–302.
Alasmary, M. Y. (2021). Antimicrobial resistance patterns and ESBL of uropathogens isolated from adult females in Najran region of Saudi Arabia. Clinical Practice, 11, 650–658.
Alibi, S., Ferjani, A., & Boukadida, J. (2015). Molecular characterization of extended spectrum beta-lactamases produced by Klebsiella pneumoniae clinical strains from a Tunisian Hospital. Médecine et Maladies Infectieuses, 45(4), 139–143.
Al-Mayahie, S., & Al Kuriashy, J. J. (2016). Distribution of ESBLs among Escherichia coli isolates from outpatients with recurrent UTIs and their antimicrobial resistance. The Journal of Infection in Developing Countries, 10(6), 575–583.
Benyagoub, E., Alkhudhairy, M. K., Benchaib, S. M., Zaalan, A., Mekhfi, Y., Teyebi, N., Razni, D., & Bendada, F. (2021). Isolation frequency of uropathogenic strains and search for ESBL producing Enterobacteriaceae isolated from patients with UTI in Bechar (Algeria). Anti-Infective Agents, 19(3), 303–316.
Critchley, I. A., Cotroneo, N., Pucci, M. J., & Mendes, R. (2019). The burden of antimicrobial resistance among urinary tract isolates of Escherichia coli in the United States in 2017. PloS One, 14(12), 0220265.
Dash, N. R., Albataineh, M. T., Alhourani, N., Khoudeir, A. M., Ghanim, M., Wasim, M., & Mahmoud, I. (2018). Community-acquired urinary tract infections due to extended-spectrum β-lactamase-producing organisms in United Arab Emirates. Travel Medicine and Infectious Disease, 22, 46–50.
De Angelis, G., Del Giacomo, P., Posteraro, B., Sanguinetti, M., & Tumbarello, M. (2020). Molecular mechanisms, epidemiology and clinical importance of β-lactam resistance in Enterobacteriaceae. International Journal of Molecular Sciences, 21, 5090.
El bouamri, M. C., Arsalane, L., Zerouali, K., Katfy, K., El kamouni, Y., Zouhair, S. (2015). Molecular characterization of extended spectrum β-lactamase-producing Escherichia coli in a university hospital in Morocco, North Africa. African Journal of Urology, 21, 161–166.
Gharavi, M. J., Zarei, J., Roshani-Asl, P., Yazdanyar, Z., Sharif, M., & Rashidi, N. (2021). Comprehensive study of antimicrobial susceptibility pattern and extended spectrum beta-lactamase (ESBL) prevalence in bacteria isolated from urine samples. Scientific Reports, 11(1), 578.
Halabi, M. K., Lahlou, F. A., Diawara, I., Adouzi, Y. E., Marnaoui, R., Benmessaoud, R., & Smyej, I. (2021). Antibiotic resistance pattern of extended spectrum beta lactamase producing Escherichia coli isolated from patients with urinary tract infection in Morocco. Frontiers in Cellular and Infection Microbiology, 2021, 720701.
Hantalo, A. H., Taassaw, K. H., Solomon, F. B., & Woldeamanuel, Y. (2020). Isolation and antibiotic susceptibility pattern of bacterial uropathogens and associated factors among adult people living with HIV/AIDS attending the HIV Center at Wolaita Sodo University Teaching Referral Hospital, South Ethiopia. HIV/AIDS: Research and Palliative Care, 12, 799–808.
Hassuna, N. A., Khairalla, A. S., Farahat, E. M., Hammad, A. M., & Abdel-Fattah, M. (2020). Molecular characterization of extended-spectrum β-lactamase producing E. coli recovered from community-acquired urinary tract infections in Upper Egypt. Scientific Reports, 10, 2772.
Jarlier, V., Nicolas, M. H., Fournier, G., & Philippon, A. (1988). Extended broad-spectrum beta-lactamases conferring transferable resistance to newer beta-lactam agents in Enterobacteriaceae: Hospital prevalence and susceptibility patterns. Reviews of Infectious Diseases, 10, 867–878.
Kharrat, M., Chebbi, Y., Tanfous, F. B., Lakhal, A., Ladeb, S., Othmen, T. B., & Achour, W. (2018). Extended spectrum beta-lactamase-producing Enterobacteriaceae infections in hematopoietic stem cell transplant recipients: Epidemiology and molecular characterization. International Journal of Antimicrobial Agents, 52(6), 886–892.
Kunishima, H., Ishibashi, N., Wada, K., Oka, K., Takahashi, M., Yamasaki, Y., Aoyagi, T., Takemura, H., Kitagawa, M., & Kaku, M. (2019). The effect of gut microbiota and probiotic organisms on the properties of extended spectrum beta-lactamase producing and carbapenem resistant Enterobacteriaceae including growth, beta-lactamase activity and gene transmissibility. Journal of Infection and Chemotherapy, 25(11), 894–900.
Lin, S. P., Liu, M. F., Lin, C. F., & Shi, Z. Y. (2012). Phenotypic detection and polymerase chain reaction screening of extended-spectrum b-lactamases produced by Pseudomonas aeruginosa isolates. Journal of Microbiology, Immunology and Infection, 45(3), 200–207.
Magiorakos, A. P, Srinivasan, A., Carey, R. B., Carmeli, Y., Falagas, M. E., Giske, C. G., Harbarth, S., Hindler, J. F., Kahlmeter, G., Olsson-Liljequist, B., Paterson, D. L., Rice, L. B, Stelling, J., Struelens, M. J., Vatopoulos, A., Weber, J. T., & Monnet, D. L. (2012). Multidrug resistant, extensively drug-resistant and pan-drug-resistant bacteria: An international expert proposal for interim standard definitions for acquired resistance. Clinical Microbiology and Infection, 18, 268–281.
Mazzariol, A., Bazaj, A., & Cornaglia, G. (2017). Multidrug-resistant Gram-negative bacteria causing urinary tract infections: A review. Journal of Chemotherapy, 29(suppl. 1), 2–9.
Mechai, A., Debabza, M., Fares, R., Metrouh, R., & Amra, A. (2020). Antibiotic susceptibility pattern and phenotypic characterization of extended-spectrum-beta-lactamase-producing Enterobacteriaceae isolated from various clinical samples. Environmental Engineering and Management Journal, 19(12), 2139–2146.
Mohammed, M. A., Alnour, T. M. S., Shakurfo, O. M., & Aburass, M. M. (2016). Prevalence and antimicrobial resistance pattern of bacterial strains isolated from patients with urinary tract infection in Messalata Central Hospital, Libya. Asian Pacific Journal of Tropical Medicine, 9(8), 771–776.
Muthupandian, S., Ramachandran, B., & Barabadic, H. (2018). The prevalence and drug resistance pattern of extended spectrum β-lactamases (ESBLs) producing Enterobacteriaceae in Africa. Microbial Pathogenesis, 114, 180–192.
Nabti, L. Z, Sahli, F., Radji, N., Mezaghcha, W., Semara, L., Aberkane, S., Lounnas, M., Solassol, J., Didelot, M. N., Jean-Pierre, H., Dumont, Y., & Godreuil, S. (2019). High prevalence of multidrug-resistant Escherichia coli in urine samples from inpatients and outpatients at a tertiary care hospital in Setif, Algeria. Microbial Drug Resistance, 25(3), 386–393.
Natoubi, S., Barguigua, A., Diawara, I., Timinouni, M., Rakib, K., Amghar, S., & Zerouali, K. (2020). Epidemiology of extended-spectrum β-lactamases and carbapenemases producing Enterobacteriaceae in Morocco. Journal of Contemporary Clinical Practice, 6(2), 75–85.
Rahal, K. (2005). Standardisation de l’antibiogramme en Médecine Humaine à l’échelle nationale selon les recommandations de l’OMS. 4th edition. Algeria.
Rania, Y. Shash, L., Elshimy, A. A., Soliman, M. Y., & Mosharafa, A. A. (2019). Molecular characterization of extended-spectrum β-lactamase Enterobacteriaceae isolated from Egyptian patients with community- and hospital-acquired urinary tract infection. American Journal of Tropical Medicine and Hygiene, 100(3), 522–528.
Raya, G. B., Dhoubhadel, B. G., Shrestha, D. P., Raya, S., Laghu, U., Shah, A., Raya, B. B., Kafle, R., Parry, C. M., & Ariyoshi, K. (2020). Multidrug-resistant and extended-spectrum beta-lactamase-producing uropathogens in children in Bhaktapur, Nepal. Tropical Medicine and Health, 48(1), 65.
Sbiti, M., Lahmadi, K., & Louzi, L. (2017). Profil épidémiologique des entérobactéries uropathogènes productrices de bêta-lactamases à spectre élargi. The Pan African Medical Journal, 28, 29.
Somily, A. M., Habib, H. A., Absar, M., Arshad, M., Manneh, K., Subaie, S. S. A., Hedaithy, M. A. A., Sayyed, S. B., Shakoor, Z., & Murray, T. F. (2014). ESBL-producing Escherichia coli and Klebsiella pneumoniae at a tertiary care hospital in Saudi Arabia. Journal of Infection in Developing Countries, 8(9), 1129–1136.
Tayh, G., Laham, N. A., Yahia, H. B., Sallem, R. B., Elottol, A. E. K. Y., & Slama, K. B. (2019). Extended-spectrum β-lactamases among Enterobacteriaceae isolated from urinary tract infections in Gaza Strip, Palestine. BioMed Research International, 2019, 4041801.
Tekele, S. G., Teklu, D. S., Tullu, K. D., Birru, S. K., & Legese, M. H. (2020). Extended-spectrum betalactamase and AmpC beta-lactamases producing gram negative bacilli isolated from clinical specimens at international clinical laboratories, Addis Ababa, Ethiopia. PLoS One, 15(11), e0241984.
Tooke, C. L., Hinchliffe, P., Bragginton, E. C., Colenso, C. K., Hirvonen, V. H. A., Takebayashi, Y., & Spencer, J. (2019). β-Lactamases and β-lactamase inhibitors in the 21st century. Journal of Molecular Biology, 431(18), 3472–3500.
Zenati, F., Barguigua, A., Nayme, K., Benbelaïd, F., Khadir, A., Bellahsene, C., Bendahou, M., Hafida, H., & Timinouni, M. (2019). Characterization of uropathogenic ESBL-producing Escherichia coli isolated from hospitalized patients in Western Algeria. Journal of Infection in Developing Countries, 13(4), 291–302.
Published
2023-04-05
Issue
Section
Articles
This work is licensed under a Creative Commons Attribution 4.0 International License.
