Investigation of Extended Spectrum Beta Lactamase Frequency in Escherichia coli and Klebsiella pneumoniae Strains Isolated From Individuals Affected By a Major Earthquake

Abstract

Aim: Extended-Spectrum β-Lactamase (ESBL) - producing Escherichia coli (E.coli) and Klebsiella pneumoniae (K.pneumoniae) are threatening pathogens which are more resistant to antibiotics in healthcare settings all around the world. The spread of these pathogens may be triggered by natural disasters such as earthquake and flood. Material and Method: A total of 3129 subjects were included in this study and evaluated retrospectively between January 2023 and July 2024 just before and after a major earthquake. VITEK® 2 compact automatized system was used to identify the strains. Extendedspectrum β-lactamase production was determined by double disc synergy test and combine disc synergy test. VITEK® 2 compact automatized system was used to determine the antibiotic resistance of strains. All statistical analyses were performed using IBM Statistical Package for Social Sciences (SPSS) program. Chi-square test was applied in comparing the variables between the groups. Statistical significance threshold was found to be P value of <0.05. Results: Nine hundred and fifty two E.coli and 355 K.pneumoniae strains were isolated from 3129 clinical samples. The 478 E. coli (50.21%) and 102 K.pneumoniae strains (28.73%) were found to be ESBL-positive. ESBL-producing E.coli strains were mostly resistant to cefuroxime (97.48%), ceftriaxone (84.51%) and 97.05% resistance rate was determined in ESBL-positive K.pneumoniae strains against ceftriaxone. Conclusion: Although ESBL positivity was high in E.coli strains and not significantly different when compared with literature, it was found to be relatively moderate in K.pneumoniae strains. It can be said that despite the major earthquake disaster, these findings are promising.

Keywords

• ESBL
• E.coli
• K.pneumoniae
• nosocomials; antibiotic resistance

References

1. 1. Akenten CW, Ofori LA, Khan NA, et al. Prevalence, characterization, and antimicrobial resistance of extendedspectrum beta-lactamase-producing Escherichia coli from domestic free-range poultry in Agogo, Ghana. Foodborne Pathog Dis. 2023;20(2):59–66.
2. 2. Özçerezci Ö, Savcı Ü. Yenidoğan Yoğun Bakım Ünitesinde Preterm ve Term Bebeklerde Genişlemiş Spektrumlu BetaLaktamaz Üreten Gram-Negatif Bakteri Enfeksiyonlarının Değerlendirilmesi. J Pediatr Emerg Intensive Care Med. 2019;6:91–97.
3. 3. Maslikowska, JA, Walker, SA, Elligsen, M, et al. Impact of infection with extended-spectrum beta-lactamase-producing Escherichia coli or Klebsiella species on outcome and hospitalization costs. J Hosp Infect. 2016;92:33–41.
4. 4. Antimicrobial Resistance Collaborators. Global burden of bacterial antimicrobial resistance in 2019: a systematic analysis. T he Lancet. 2022;399(10325):629–55.
5. 5. Knothe H, Shah P, Krcmery V, et al. Transferable resistance to cefotaxime, cefoxitin, cefamandole and cefuroxime in clinical isolates of Klebsiella pneumoniae and Serratia marcescens. Infection. 1983;11(6):315–7.
6. 6. Pitout JD. Infections with extended-spectrum β-lactamaseproducing Enterobacteriaceae: changing epidemiology and drug treatment choices. Drugs. 2010;70:313–33.
7. 7. Ouedraogo A. Prévalence, circulation et caractérisation des bactéries multirésistantes au Burkina Faso [thesis]. Spécialité: Biologie Santé. France: HAL Id: tel-01476152;2017. French.
8. 8. Ahmadi M, Ranjbar R, Behzadi P, et al. Virulence factors, antibiotic resistance patterns, and molecular types of clinical isolates of Klebsiella pneumoniae. Expert Rev Anti Infect Ther. 2022;20(3):463–472.

9. 9. Martin RM, Bachman MA. Colonization, infection, and the accessory genome of Klebsiella pneumoniae. Front Cell Infect Microbiol. 2018;8:4.
10. 10. World Health Organization, 7th Feb 2018 report. (Internet) [Available from: https://www.who.int]
11. 11. Bagley ST. Habitat association of Klebsiella species. Infect Control. 1985;6:52–58.
12. 12. Hyun M, Lee JY, Kim HA, et al. Comparison of Escherichia coli and Klebsiella pneumoniae acute pyelonephritis in Korean patients. Infect Chemother. 2019;51(2):130–141.
13. 13. Kayastha K, Dhungel B, Karki S, et al. Extended-spectrum β-lactamase-producing Escherichia coli and Klebsiella species in pediatric patients visiting International Friendship Children’s hospital, Kathmandu, Nepal. J Infect Dis. 2020;13:1178633720909798.
14. 14. Allocati N, Masulli M, Alexeyev MF, et al. Escherichia coli in Europe: an overview. Int J Environ Res Public Health. 2013;10(12):6235–54.
15. 15. Akyar I, Kocagöz S, Kocagöz T, et al. Beş yılda izole edilen 15434 Escherichia coli ve 3178 Klebsiella spp. suşunda genişlemiş spektrumlu beta-laktamaz üretiminin yıllara, kliniklere ve örnek türlerine dağılımı. ANKEM Derg. 2010;24:34–41. Kafkas J Med Sci 2025; 15(2):219–228227
16. 16. Gupta V. An update on newer beta-lactamases. Indian J Med Res. 2007;126(5):417–27. PMID:18160745.
17. 17. Amana MD, Jacob ZK, Boukaré ZE, et al. Resistances to the oxyimino-cephalosporins by CTX-M-15 producing Klebsiella isolated from the urines samples of patients in the University Hospital Complex Paediatric Charles De Gaulle (CHUPCDG) of Ouagadougou in Burkina Faso. J Asian Sci Res. 2013;3(9):882–890.
18. 18. Albayrak N, Kaya Ş. Çeşitli klinik örneklerden izole edilen Escherichia coli ve Klebsiella pneumoniae suşlarının genişlemiş spektrumlu beta laktamaz üretimleri ve antibiyotik direnç oranları. Türk Mikrobiyoloji Cemiyeti Dergisi. 2009;39:16–21.
19. 19. The European committee on antimicrobial susceptibility testing. Breakpoint tables for interpretation of MICs and zone diameters. Version 9.0; 2019. http://www.eucast.org
20. 20. Tunçcan ÖG, Keten DT, Dizbay M, et al. Hastane kaynaklı Escherichia coli ve Klebsiella suşlarının ertapenem ve diğer antibiyotiklere duyarlılığı. ANKEM Derg. 2008;22:188–192.
21. 21. Afzal MA. Antibiotic resistance pattern of Escherichia coli and Klebsiella spe cies in Pakistan: a brief overview. J Microb Biochem Technol. 2017;9:277–9.
22. 22. Murray CJ, Ikuta KS, Sharara F. Global burden of bacterial antimicrobial resistance in 2019: A systematic analysis. Lancet. 2022:399;629–655.
23. 23. Ahmadishooli A, Davoodian P, Shoja S, et al. Frequency and Antimicrobial Susceptibility Patterns of Diabetic Foot Infection of Patients from Bandar Abbas District, Southern Iran. J Pathog. 2020;2020:1057167.
24. 24. Vazin A, Shahriarirad R, Azadeh N, et al. Incidence, clinicomicrobiological characteristics, risk factors, and treatment outcomes of bacterial infections following liver transplantation in pediatrics: A retrospective cohort study. Arch Pediatr Infect Dis. 2022;10(4).
25. 25. Forouzani F, Khasti T, Manzouri L, et al. Resistance pattern of isolated microorganisms from 783 clinical specimen cultures in patients admitted to Yasuj Educational Hospitals, Iran. BMC Microbiol. 2023;23:205.
26. 26. Parmar D, Prakash N, Umrania V, et al. The study of the prevalence of different microorganisms in clinical specimens at a tertiary care hospital. Proc Natl Conf Innov Biol Sci (NCIBS). 2020 Apr 10.
27. 27. Gürbüz M, Türkekul Şen E, Demir C, et al. Afyonkarahisar Sağlık Bilimleri Üniversitesi Sağlık Uygulama ve Araştırma Merkezi Yatan Hasta Kümülatif Antibiyotik Duyarlılık Raporu (2020). Türk Mikrobiyoloji Cemiyeti Dergisi. 2021;51(4):38292.
28. 28. Kawa DE, Tickler IA, Tenover FC, et al. Characterization of beta-lactamase and fluoroquinolone resistance determinants in Escherichia coli, Klebsiella pneumoniae, and Pseudomonas aeruginosa isolates from a tertiary hospital in Yola, Nigeria. Trop Med Infect Dis. 2023;8(11):500.
29. 29. Şenol FF, Bahçeci İ, Aytaç Ö, et al. Çeşitli klinik örneklerden izole edilen gram negatif gsbl pozitif bakterilerin antibiyotiklere direnç oranları. Turk J Clin Lab. 2021;4:451–457.
30. 30. Bozok T, Öztürk A. Niğde ilinde üçüncü basamak bir hastaneden izole edilen bakterilerin tür dağılımı ve antibiyotik duyarlılıkları: Üç yıllık değerlendirme. Mersin Univ Saglık Bilim Derg. 2023;16(1):22–39.
31. 31. Demirağ K, Özden M, Denk A, et al. Klinik Örneklerden izole Edilen Gram Negatif Bakterilerde Siprofloksasin Direncinin Retrospektif Olarak Değerlendirilmesi. Türk Mikrobiyoloji Dergisi. 2003;33:236–241.
32. 32. Özmen E, Geyik MF, Çelen MK, et al. Yatan hastalardan izole edilen Gram negatif bakteriler ve antibiyotik dirençlerinin değerlendirilmesi. Duzce Medical Journal. 2010;12(3):32–39.
33. 33. Altoparlak Ü, Özbek A, Aktaş F. Klinik Örneklerden İzole Edilen Gram Negatif Çomaklarda İzepamisinin Antibakteriyel Aktivitesinin Diğer Aminoglikozidlerle Karşılaştırılması. Türk Mikrobiyoloji Cemiyeti Dergisi. 2003;33:19–23.
34. 34. Ali SA, Mandal S, Georgalas A, et al. A pattern of antibiotic resistance in gram-negative rods causing urinary tract infection in adults. Cureus. 2021;13(1):e12977.
35. 35. Orhan Z, Kayış A, Küçük B, et al. Yoğun Bakım Üniteleri ve Yataklı Servislerde Yatan Hastaların Kültürlerinden Sık İzole Edilen Gram Negatif Bakteriler ve Antibiyotik Dirençlerinin Retrospektif Olarak Değerlendirilmesi. Sakarya Tıp Dergisi. 2022;12(4):596–602.
36. 36. Avcıküçük H, Altın N. İdrar Kültürlerinden İzole Edilen Bakteriler ve Çeşitli Antibiyotiklere Karşı Direnç Durumları. Klimik Dergisi. 2022;35(2):95–102.
37. 37. Mangram AJ, Horan TC, Pearson ML, et al. Guideline for Prevention of Surgical Site Infection, 1999. Infection Control & Hospital Epidemiology. 1999;20(4):247–280.
38. 38. Negut I, Grumezescu V, Grumezescu AM. Treatment Strategies for Infected Wounds. Molecules. 2018;23(9):2392.
39. 39. Cardona AF, Wilson SE. Skin and soft-tissue infections: a critical review and the role of telavancin in their treatment. Clin Infect Dis. 2015;61 Suppl 2:S69–78.
40. 40. Watanabe N, Koayam S, Taji Y, et al. Direct microorganism species identification and antimicrobial susceptibility tests from positive blood culture bottles using rapid Sepsityper Kit. J of Inf Chem. 2022;28(4):563–568.
41. 41. Alharbi AS. Bacteriological profile of wound swab and their antibiogram pattern in a tertiary care hospital, Saudi Arabia. Saudi Med J. 2022;43(12):1373–82.
42. 42. Ali KM, Al-Jaff BM. Source and antibiotic susceptibility of gram-negative bacteria causing superficial incisional surgical site infections. Int J Surg Open. 2021;30:100318.
43. 43. Tanrıverdi Çaycı Y, Torun EG, Bilgin K, et al. Yara Yeri Örneklerinden İzole Edilen Etkenler ve Antibiyotik Direnç Profilleri. Düzce Üniversitesi Sağlık Bilimleri Enstitüsü Dergisi. 2021;11(2):123–128.
44. 44. World Health Organization. Global antimicrobial resistance and use surveillance system (GLASS) report 2022.
45. 45. CDC, A. Antibiotic resistance threats in the United States. US Department of Health and Human Services: Washington, DC, USA. 2019;1:67–100. Kafkas J Med Sci 2025; 15(2):219–228228
46. 46. Będzichowska A, Przekora J, Stapińska-Syniec A, et al. Frequency of infections caused by ESBL-producing bacteria in a pediatric ward: single-center five-year observation. Arch Med Sci. 2019;15(3):688–93.
47. 47. Aykan, ŞB, Çiftci İH. Türkiye’de idrar kültürlerinden izole edilen Escherichia coli suşlarının antibiyotiklere direnç durumu: Bir meta-analiz. Mikrobiyol Bul. 2013;47(4):603–18.
48. 48. Bayraktar B, Pelit S, Bulut ME, et al. Trend in Antibiotic Resistance of Extended-Spectrum Beta-Lactamase-Producing Escherichia Coli and Klebsiella Pneumoniae Bloodstream Infections. Sisli Etfal Hastan Tip Bul. 2019;53(1):70–75.
49. 49. Parlak M, Çıkman A, Bektaş A, et al. Escherichia coli ve Klebsiella pneumoniae suşlarında genişlemiş spektrumlu betalaktamaz üretimi ve antibiyotiklere direnç: beş yıllık izlem. Sakarya Tıp Dergisi. March. 2012;2(1):11–15.
50. 50. Onuk S, Esmaoğlu Çoruh A, Ulu Kılıç A, et al. The frequency of ESBL producing bacterial infections and related antimicrobial susceptibility in ICU patients: A five-year longitudinal study. Ann Clin Anal Med. 2023;14:26–30.
51. 51. Bursal B, Özdemir AA, Topal N, et al. Insights into ExtendedSpectrum Beta-Lactamase Producing Bacteria Related Urinary Tract Infections in Children: A Single Center Experience. J Pediatr Inf. 2025;19(1):13–23.
52. 52. Akıneden A, Türkel S, Çiçek C. Antimicrobial susceptibility patterns and extended-spectrum β-Lactamase production by enterobacterales in a tertiary hospital. Aksaray Üniversitesi Tıp Bilimleri Dergisi. 2025;5(1):1–6.
53. 53. Garba Z, Kaboré B, Bonkoungou IJO, et al. Phenotypic Detection of Carbapenemase and AmpC-β-Lactamase Production among Extended Spectrum β-Lactamase (ESBL) - Producing Escherichia coli and Klebsiella spp. Isolated from Clinical Specimens. Antibiotics (Basel). 2023;13(1):31.
54. 54. Coşkun MV, Uyanık MH, Ağan İ, et al. Hastanede Yatan Hastaların Üriner Sistem İnfeksiyonlarından İzole Edilen Genişlemiş Spektrumlu Beta-Laktamaz Üreten Klebsiella Pneumoniae ve Escherichia Coli Suşlarının Fosfomisin ve Nitrofurantoine Duyarlılıklarının Araştırılması. Ankem Derg. 2016;30(2):37–41.
55. 55. Wani FA, Bandy A, Alenzi MJS, et al. Resistance Patterns of Gram-Negative Bacteria Recovered from Clinical Specimens of Intensive Care Patients. Microorganisms. 2021;9:2246.
56. 56. Aydoğmuş S, Kaya Kılıç E. Determination of antibiotic resistance rates of Escherichia coli and Klebsiella pneumoniae isolates, which are the causative agents of urinary tract infection in pregnant women. Anatolian Curr Med J. 2023;5(2):97–101.
57. 57. Öner SZ, Kaleli İ, Demir M, et al. Kan kültüründen izole edilen gram negatif çomaklar ve antimikrobiyal direnç. Türk Mikrobiyoloji Cemiyeti Dergisi. 2024;54(4):274–281.
58. 58. Keskin BH, Çalışkan E, Kaya S, et al. Üriner sistem enfeksiyonlarında etken bakteriler ve antibiyotik direnç oranları. Türk Mikrobiyoloji Cemiyeti Dergisi. 2021;51(3):254–62.