More Information

Submitted: January 02, 2024 | Approved: January 11, 2024 | Published: January 12, 2024

How to cite this article: Alkhodari K, Al-Shurafa Y, AL-louh H, Lubbad R. Trends of Antibiotic Resistance among Uropathogens in Medical vs. Non-Medical Departments of Al-Shifa Medical Complex in Gaza Strip: A Retrospective, Cross-Sectional Study. Int J Clin Microbiol Biochem Technol. 2024; 7: 001-005.

DOI: 10.29328/journal.ijcmbt.1001028

!-- Copyright -->

Copyright License: © 2024 Alkhodari K, et al. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Keywords: Anti-bacterial agents; Urinary tract infections; Antibiotic resistance; Uropathogens; Palestine; Gaza strip

Abbreviations: UTI: Urinary Tract Infections

 FullText PDF

Trends of Antibiotic Resistance among Uropathogens in Medical vs. Non-Medical Departments of Al-Shifa Medical Complex in Gaza Strip: A Retrospective, Cross-Sectional Study

Khaled Alkhodari1*, Yasmin Al-Shurafa2, Hammam AL-louh3 and Rafat Lubbad3

1Internal Medicine Resident, Department of Medicine, Al Shifa Medical Complex, Gaza, Palestine
2Clinical Pharmacist, Department of Medicine, Al Shifa Medical Complex, Gaza, Palestine
3Consultant Internist, Department of Medicine, Al Shifa Medical Complex, Gaza, Palestine

*Address for Correspondence: Khaled Alkhodari, Internal Medicine Resident, Department of Medicine, Al Shifa Medical Complex, 333999 Gaza, Strip, Palestine, Email: Khaled.Alkhodari@gmail.com

Antibiotic resistance is a growing global crisis, straining healthcare systems and leaving us with limited options to combat drug-resistant bacteria. This retrospective, cross-sectional study examines the prevalence of antibiotic resistance patterns among urinary tract infections (UTIs) in Al-Shifa Hospital’s medical departments in comparison with non-medical departments using data from microbiology laboratory archives over a one-year period.

From the examined urine cultures about 25% were obtained from internal medicine departments and double the number was obtained from non-medical departments. The positive rate was around 35% and about two-thirds of the samples were collected from female patients.

Among all departments, Enterobacteriaceae spp. were found to be the most frequently isolated uropathogens, accounting for 80% of cases. However, resistance rates varied depending on the specific organism and antibiotic used. For instance, E. coli showed a resistance rate of only 5% against meropenem, while amoxicillin-clavulanic acid exhibited a resistance rate exceeding 95%.

Importantly, the study revealed a significant disparity in resistance rates between medical and non-medical departments, specifically concerning third-generation cephalosporins. In internal medicine departments, resistance rates were alarmingly high, with cefotaxime, ceftriaxone, and ceftazidime showing resistance rates of 75%, 75% and 66.5% respectively. In contrast, non-medical departments displayed lower resistance rates, approximately 60%, 60% and 40%, respectively.

In summary, this research sheds light on the escalating problem of antibiotic resistance in UTIs and emphasizes the discrepancy in resistance rates between medical and non-medical departments. Urgent efforts are required to address this issue and find effective solutions to prevent the rise of untreatable bacterial infections.

Urinary tract infections are one of the most common bacterial infections among the population [1]. The clinical spectrum of urinary tract infection is wide as it can be simple cystitis to complicated infections with systemic response and sepsis with shock sometimes [2]. Urinary tract infection is defined by the Food and Drug Administration as a clinical syndrome with pyuria and documented uropathogens on blood or urine culture associated with local and systemic signs and symptoms that occur in the presence of functional or anatomical abnormality of the urinary tract or the presence of urinary catheter [3].

Antibiotic resistance is an alarming threat to healthcare systems. After the presence of antibiotics as a solution for life-threatening infections, their resistance poses a serious threat to their effectiveness in treating infectious diseases. The resistance is increasing with time leaving us with limited choices to face bacteria [4,5].

The issue of antibiotic resistance is not only affecting patients but also increasing the burden on health systems in many aspects. This has led to an increase in infectious disease burden by increasing treatment costs, hospital stays, and morbidity and mortality rates. For example, in the United States, bacterial infections cost about 55 billion dollars per year according to the CDC, and in Europe, it costs about nine billion euros annually [6-8]. Additionally, by the year 2050, it was estimated that antibiotic-resistant bacteria will be one of the ten leading causes of death globally with more deleterious effects on developing countries [9].

One of the main causes of increased resistance in the world is the overuse and misuse of antibiotics, which has led to the generation of multi-drug resistant bacteria (MDR), extensively drug-resistant bacteria (XDR), and pan-resistant bacteria (PDR) that are not responsive to the usual existing antibiotics [10]. On the other hand, bacteria are evolving antibiotic-resistant organisms faster than researchers can develop new antibiotics [11].

Urinary tract infections (UTIs) are among the leading causes of admissions to medical wards in the Gaza Strip. Increasingly, patients are admitted with complications of (UTI) with sepsis and septic shock with increasing hospital stays due to multi-drug resistant organisms. Unfortunately, there are still no local guidelines for managing such infections due to the relative lack of antibiogram studies. This study is part of the initiation of local guidelines and aims to study the most common organisms and rates of antibiotic resistance to choose the most appropriate empirical antibiotic for (UTIs).

A retrospective hospital-based; cross-sectional study that has included urine sample results from patients admitted to Al-Shifa hospital departments in the Gaza Strip. The departments were divided into medical departments and other non-medical departments which included general surgery, vascular surgery, orthopedic surgery, obstetrics and gynecology, intensive care, and outpatient departments.

Data were manually collected from the microbiology laboratory database for the year 2022. We included all urine culture results that are assigned to departments. Urine sample results that were not labeled to a department were excluded.

Urine samples were collected from patients as mid-stream urine samples and sent to the lab as soon as possible within one hour. Then the samples are cultured on nutrient agar plates by a 10 µl calibrated loop and plated on blood and McConkey agar. Plates were then incubated at 370C at the laboratory. Subsequently, the plates were examined for growth and colonies and classified as positive and negative according to WHO recommendations [12].

Data were classified into categorical and numerical data types and analysis was done using SPSS version 23.

Ethical approval was obtained from the head of the hospital and the research committee to use the collected microbiology laboratory data.

Urine culture results from all departments (n = 3362) were examined. About a quarter (24.2% n = 815) were collected from medical departments and another (24.3% n = 820) was not assigned to any department (that was excluded from the analysis). The remaining half (51.3% n = 1727) was obtained from non-medical departments. Around 35% (n = 885) of all urine cultures were assigned as positive with the majority 66% (n = 586) obtained from female patients. The following analysis will compare findings in the internal medicine departments and other departments.

Regarding urine samples that were obtained from internal medicine departments, a total of 813 specimens were investigated; about 42% (n = 345) of cultures were positive with most of them cultured from female patient samples, about 71% (n = 245) Table 1.

Table 1: Positive results analysis among sex.
Positive results analysis Sex Total
male female
Internal medicine departments Count 99 246 345
% within Result 28.7% 71.3% 100.0%
% within Sex 36.1% 45.7% 42.5%
% of Total 12.2% 30.3% 42.5%
Non-medical departments Count 198 341 539
% within Result 36.7% 63.3% 100.0%
% within Sex 30.8% 31.5% 31.3%
% of Total 11.5% 19.8% 31.3%

On the other hand, from non-medical departments, 1727 urine samples were cultured with about 31% (n = 539) of samples coming back positive; also, of which most of them were collected from female patients (63%, n = 341) Table 1.

The distribution of uropathogens that have been isolated from all departments was relatively the same with the most commonly isolated organism being E. coli at about 51.6% (n = 456), which is followed by Klebsiella at about 24.9% (n = 220), pseudomonas pp. around 7% (n = 61), streptococcus 5% (n = 43), and P. Mirabilis 3.4% (n = 30). Enterobacteriaceae spp. (E. Coli, K. pneumonia, P. Mirabilis) formed the vast majority of the isolated uropathogens with about 84% (n = 289) in medical departments and 78% (n = 418) in the non-medical departments Table 2.

Table 2: The distribution of uropathogens among departments.
  Internal medicine departments Non-medical departments
  Frequency Percent Frequency Percent
E. Coli 187 54.2 273 50.6
K.pneumonia 87 25.2 130 24.1
P. Mirabilis 15 4.3 15 2.8
Acinetobacter spp 2 .6 7 1.3
P. aeruginosa 17 4.9 44 8.1
Streptococcus spp 16 4.6 27 5.0
S. Aureus 4 1.2 15 2.8
Enterobacter Spp 0 0 1 0.2
Candida 17 4.9 28 5
Total 345 100 540 100

The antibiogram of Enterobacteriaceae spp isolated from medical departments has a wide range. For example, meropenem was the most sensitive antibiotic with a sensitivity of 95.9% (n = 47) for E. coli, 100% (n = 2) for proteus, and 84% (n = 16) for K. pneumoniae. However, the resistance rate is very high against the studied cephalosporins and ciprofloxacin against E. Coli with 90% (n = 19), 84.5% (n = 49), 77% (n = 138), 75.6% (n = 118), 75.6% (n = 133), 66.5% (n = 115), 67% (n = 30) for cefazolin, cephalexin, cefuroxime, cefotaxime, ceftriaxone, ceftazidime, and ciprofloxacin; respectively Table 3.

Table 3: Antibiotic resistance rates in internal medicine departments.
  E. Coli K. Pneumonia Proteus
  S I R S I R S I R
  N % N % N % N % N % N % N % N % N %
Cefazolin 2 10.5 0 0 19 89.5 1 10 0 0 9 90 \ \ \ \ \ \
Cefuroxime 40 22.3 1 0.6 138 77.1 9 10.7 1 1.2 74 88.1 6 40 0 0 9 60
Ceftazidime 51 29.5 7 4 115 66.5 27 33.8 6 7.5 47 85.8 8 57.1 1 7 5 35.7
Cefotaxime 38 24.2 0 0 118 75.6 11 14.5 1 1.3 64 84.2 9 60 0 0 6 40
Ceftriaxone 42 23.9 1 0.6 133 75.6 10 11.9 1 1.2 73 86.9 9 60 0 0 6 40
Cephalexin 8 13.8 1 1.7 49 84.5 3 10.3 0 0 26 89.7 2 25 0 0 6 75
Gentamycin 78 52.7 10 6.8 60 40.5 35 50 2 2.9 33 47.1 5 41.7 0 0 7 58.3
Amikacin 111 75 9 6.1 28 18.9 51 71.8 2 2.8 18 25.4 9 64.3 1 7.1 4 28.6
Ciprofloxacin 47 44.3 6 5.7 30 66.7 11 24.4 4 8.9 30 66.7 1 14.3 0 0 6 85.7
Doxycycline 47 44.3 6 5.7 53 50 11 24.4 4 8.9 30 66.7 1 14.3 0 0 6 85.7
Trimethoprim/ Sulfamethoxazole 6 22.2 0 0 21 77.8 3 30 0 0 7 70 0 0 0 0 2 100
Piperacillin/ Tazobactam 4 100 0 0 0 0 2 100 0 0 0 0 \ \ \ \ \ \
Meropenem 47 95.9 0 0 2 4.1 16 84.2 0 0 3 15.8 2 100 0 0 0 0
Colistin 30 18.1 2 1.2 134 80.7 22 27.5 0 0 58 72.5 4 28.6 0 0 10 71.4
amoxicillin-clavulanic acid 0 0 0 0 13 100 0 0 0 0 4 100 \ \ \ \ \ \
S:Sensitive; I: intermediate; R: Resistant; N: Number of patients; %:Percentage of patients.

On the contrary, resistance rates generally were relatively lower in departments other than internal medicine. As resistance rates were relatively lower against third-generation cephalosporins and ciprofloxacin, for example, against E. Coli with rates of 70% (n = 18), 64.7% (n = 55), 70.5% (n = 86), 60.9% (n = 142), 60% (n = 155), 41% (n = 102), 59% (n = 139) for cefazolin, cephalexin, cefuroxime, cefotaxime, ceftriaxone, ceftazidime, and ciprofloxacin; respectively Table 4.

Table 4: Antibiotic resistance rates in non-medical departments excluding internal medicine departments.
  E. Coli K. Pneumonia Proteus
  S I R S I R S I R
  N % N % N % N % N % N % N % N % N %
Cefazolin 8 30.8 0 0 18 69.2 1 11.1 0 0 8 88.9 \ \ \ \ \ \
Cefuroxime 97 37.2 2 0.8 86 70.5 35 28.7 1 0.8 86 70.5 6 40 0 0 9 60
Ceftazidime 128 51.6 18 7.3 102 41.1 48 43.2 3 2.7 60 54.1 6 42.9 0 0 8 57.1
Cefotaxime 91 39.1 0 0 142 60.9 39 34.8 1 0.9 72 64.3 7 46.7 0 0 8 53.3
Ceftriaxone 102 39.7 0 0 155 60.3 36 31.6 1 0.9 77 67.5 6 40 0 0 9 60
Cephalexin 28 32.9 2 2.4 55 64.7 11 25 1 2.3 32 72.7 2 28.6 0 0 5 71.4
Gentamycin 122 58.9 12 5.8 73 35.3 55 59.8 0 0 37 40.2 7 58.3 1 8.3 4 33.3
Amikacin 175 76.4 19 8.3 35 15.3 71 65.7 5 4.6 32 29.6 9 60 1 6.7 5 33.3
Ciprofloxacin 92 38.8 6 2.5 139 58.6 40 37.7 2 1.9 64 60.4 7 50 0 0 7 50
Doxycycline 65 48.5 5 3.7 64 47.8 31 45.9 7 10 30 44.1 3 30 0 0 7 70
Trimethoprim / Sulfamethoxazole 12 25.5 0 0 35 74.5 3 14.3 1 4.8 17 81 1 100 0 0 0 0
Piperacillin / Tazobactam 3 100 0 0 0 0 \ \ \ \ \ \ \ \ \ \ \ \
Meropenem 54 96.4 0 0 2 3.6 17 70.8 1 4.2 6 25 \ \ \ \ \ \
Colistin 5 50 0 0 5 50 1 33.3 0 0 2 66.7 \ \ \ \ \ \
amoxicillin- clavulanic acid 1 4.8 1 4.8 19 90.5 3 30 1 10 6 60 \ \ \ \ \ \
S: Sensitive; I: intermediate; R: Resistant; N: Number of patients; %: Percentage of patients.

Although Meropenem has a sensitivity rate of 96% (n = 54) against E.Coli, it has a lower rate against K.Pneumonia with 71% (n = 17) in comparison to 96% (n = 47) sensitivity rate for E.Coli and 84% (n = 16) for K.Pneumonia in medical departments Tables 3,4.

The presented discussion revolves around an investigation conducted at Al-Shifa Hospital to assess the distribution of bacteria, their antimicrobial resistance, and a comparison between medical and non-medical departments. The results indicate that the percentage of positive samples was higher in medical departments (40%) compared to non-medical departments (30%), surpassing the findings of a previous study conducted in 2006 (34%) [13].

The study reveals that E.coli remains the most common uropathogen in both medical and non-medical departments, comprising more than half of the isolated organisms throughout the years. However, there is a significant difference in antimicrobial susceptibility and resistance between medical and non-medical departments. In medical departments, E.coli displayed higher resistance rates, with 75% resistance to both cefotaxime and ceftriaxone and 66.5% resistance to ceftazidime. In contrast, the resistance rates were notably lower in non-medical departments, at approximately 60%, 60% and 40%, respectively. It is worth noting that the resistance rates in medical departments were much higher than those reported in 2006 when resistance to cefotaxime and ceftazidime was only 13%. Furthermore, E.coli resistance to ciprofloxacin experienced a sharp increase from 13% in 2006 to around 60% in all departments in 2022 [13].

A comparison with a study conducted in Al-Aqsa Hospital between 2018 and 2022, another major hospital in the Gaza Strip, revealed significant discrepancies in resistance rates. Although, cephalosporin resistance of 54%, 39%, and 53.3% for ceftriaxone, ceftazidime, and cefotaxime; respectively; which is quite similar to nonmedical departments; it was seriously higher in medical departments as it reached 75%, 65.5%, 75% [14].

Over the last two decades, huge changes have occurred to the antibiogram of bacterial isolates in the Gaza Strip. For example, E. Coli had a resistance rate of about 20% against cefuroxime and 3% against ceftazidime and ciprofloxacin. This resistance has continued to increase sharply to reach the figures in this research [15].

The observed differences in resistance between medical and non-medical departments indicate a significant gap, potentially attributed to the vulnerability of medical patients with multiple comorbidities and recurrent admissions. The study suggests further investigation to prevent the escalation of resistance in such settings.

Furthermore, the resistance rates are higher in developing countries than in developed [16]. For example, the resistance rates observed in this research were notably higher than resistance rates reported in Egypt and China. In China, E.coli resistance rates against ceftazidime and ceftriaxone were 16% and 42%, respectively [17]. Similarly, in Egypt, resistance rates were relatively lower, with 36% of E.coli being resistant to ceftriaxone and 55% resistant to ceftazidime [18].

However, it is important to consider the limitations of the study. It was a retrospective study based on microbiology laboratory reports in a resource-limited country. The lack of availability of antibiotic testing kits and the shortage of antibiotic discs resulted in missing data. Additionally, inadequate documentation led to the exclusion of some urine samples from the study. The study also lacked a thorough clinical correlation to determine if antibiotics were appropriately narrowed based on culture results, which could have aided in reducing resistance rates. These limitations highlight the need for future prospective studies to address these gaps.

The study underscores the significant difference in antibiotic resistance rates within the same institution over 20 years, and it shows a wide gap between resistance rates among different departments within the same medical complex. Therefore, it emphasizes the need for policymakers to take action to control the liberal use of antibiotics in order to face the rapidly developing antibiotic resistance rates. The authors also stress the importance of providing further clarification on the correct usage of antibiotics for appropriate indications.

Declarations

Ethics approval and consent to participate are obtained from the Ethical Committee of Al-Shifa Medical Complex with registration number 2023/0122.

Consent for publication is obtained from the director of the Al Shifa Medical Complex Internal Medicine Department.

Availability of data and material: The data are available upon request.

We are the sole authors of the article and we have taken due care to ensure the integrity of the article.

  1. Wagenlehner FME, Bjerklund Johansen TE, Cai T, Koves B, Kranz J, Pilatz A, Tandogdu Z. Epidemiology, definition and treatment of complicated urinary tract infections. Nat Rev Urol. 2020 Oct;17(10):586-600. doi: 10.1038/s41585-020-0362-4. Epub 2020 Aug 25. PMID: 32843751.
  2. Foxman B. Urinary tract infection syndromes: occurrence, recurrence, bacteriology, risk factors, and disease burden. Infect Dis Clin North Am. 2014 Mar;28(1):1-13. doi: 10.1016/j.idc.2013.09.003. Epub 2013 Dec 8. PMID: 24484571.
  3. Complicated urinary tract infections: developing drugs for treatment Revision 1. 2018. https://www.fda.gov/media/71313/download.
  4. Founou RC, Founou LL, Essack SY. Clinical and economic impact of antibiotic resistance in developing countries: A systematic review and meta-analysis. PLoS One. 2017 Dec 21;12(12):e0189621. doi: 10.1371/journal.pone.0189621. PMID: 29267306; PMCID: PMC5739407.
  5. Prestinaci F, Pezzotti P, Pantosti A. Antimicrobial resistance: a global multifaceted phenomenon. Pathog Glob Health. 2015;109(7):309-18. doi: 10.1179/2047773215Y.0000000030. Epub 2015 Sep 7. PMID: 26343252; PMCID: PMC4768623.
  6. Llor C, Bjerrum L. Antimicrobial resistance: risk associated with antibiotic overuse and initiatives to reduce the problem. Ther Adv Drug Saf. 2014 Dec;5(6):229-41. doi: 10.1177/2042098614554919. PMID: 25436105; PMCID: PMC4232501.
  7. ECDC. Surveillance of Antimicrobial Resistance in Europe. 2017. https://www.ecdc.europa.eu/sites/default/files/documents/EARS-Net-report-2017-update-jan-2019.pdf.
  8. Antibiotic resistance threats in the United States; 2013. https://www.cdc.gov/drugresistance/pdf/ar-threats-2013-508.pdf.
  9. Dadgostar P. Antimicrobial Resistance: Implications and Costs. Infect Drug Resist. 2019 Dec 20;12:3903-3910. doi: 10.2147/IDR.S234610. PMID: 31908502; PMCID: PMC6929930.
  10. Klein EY, Van Boeckel TP, Martinez EM, Pant S, Gandra S, Levin SA, Goossens H, Laxminarayan R. Global increase and geographic convergence in antibiotic consumption between 2000 and 2015. Proc Natl Acad Sci U S A. 2018 Apr 10;115(15):E3463-E3470. doi: 10.1073/pnas.1717295115. Epub 2018 Mar 26. PMID: 29581252; PMCID: PMC5899442.
  11. Ventola CL. The antibiotic resistance crisis: part 1: causes and threats. P T. 2015 Apr;40(4):277-83. PMID: 25859123; PMCID: PMC4378521.
  12. World Health Organization. Regional Office for South-East A: Guidelines on standard operating procedures for microbiology. WHO Regional Office for South-East Asia, New Delhi. 2000.
  13. Elmanama AA, Elaiwa NM, El-Ottol AE, Abu-Elamreen FH. Antibiotic resistance of uropathogens isolated from Al-Shifa hospital in Gaza Strip in 2002. J Chemother. 2006 Jun;18(3):298-302. doi: 10.1179/joc.2006.18.3.298. PMID: 17129841.
  14. Elmanama AA, El-Aydi I, Al-Reefi M, Ferwana N. Antibiogram of bacterial isolates from clinical specimens during 2018-2020 at Al-Aqsa hospital, Gaza, Palestine. The International Arabic Journal of Antimicrobial Agents. 2022; 12: 10;3823/867.
  15. Elmanama AA, Abu Tayyem NES, Sjölander I. Antimicrobial resistance of bacterial isolates from the clinical and hospital environment in Gaza Strip, Palestine: A review over 20-year. The International Arabic Journal of Antimicrobial Agents. 2021; 10.3823/859.
  16. Kot B. Antibiotic Resistance Among Uropathogenic Escherichia coli. Pol J Microbiol. 2019 Dec;68(4):403-415. doi: 10.33073/pjm-2019-048. Epub 2019 Dec 5. PMID: 31880885; PMCID: PMC7260639.
  17. Wang S, Zhao S, Zhou Y, Jin S, Ye T, Pan X. Antibiotic resistance spectrum of E. coli strains from different samples and age-grouped patients: a 10-year retrospective study. BMJ Open. 2023 Apr 12;13(4):e067490. doi: 10.1136/bmjopen-2022-067490. PMID: 37045577; PMCID: PMC10106033.
  18. Abdel Gawad AM, Ashry WMO, El-Ghannam S, Hussein M, Yousef A. Antibiotic resistance profile of common uropathogens during COVID-19 pandemic: hospital based epidemiologic study. BMC Microbiol. 2023 Jan 25;23(1):28. doi: 10.1186/s12866-023-02773-5. PMID: 36694128; PMCID: PMC9873538.