View of Multidrug Resistant Enteric Bacteria Isolated From Patients With Urinary Tract Infections

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http://annalsofrscb.ro 2588

Multidrug Resistant Enteric Bacteria Isolated From Patients With Urinary Tract Infections

Dunya Abdulwahid Muridy¹, Inam Jasim Lafta²

1 Zoonotic Diseases Unit, College of Veterinary Medicine, University of Baghdad, Iraq

2 Department of Microbiology, College of Veterinary Medicine, University of Baghdad, Iraq Correspondence: [email protected]

Abstract

Background and Objectives: Urinary tract infections (UTIs), among a wide range of microbial infections, are of a double-edged worry with health-care and economic implications. They are serious diseases that can influence various parts of the urinary tract. The aim of this study was characterization of the enteric bacteria isolated from urine of human UTIs and studying their antimicrobial sensitivity. Materials and methods: A total of 50 urine samples were collected from patients with UTIs of both genders. The isolates identification was done using routine diagnostic methods and confirmed by Vitek2. Antimicrobial susceptibility was done against 10 antimicrobials.

Results: Both genders of human were found to suffer from urinary tract problems caused by bacteria.

Out of 50 patients, 45 (90%) of the cases showed bacterial growth. Approximately, 30.43% of the human infections were found to be caused by members of the Enterobacteriaceae family. The ratio of female patients with UTIs was more than that of males, the most common bacterium isolated from human urine was E. coli, which constituted approximately 85.7% of the enteric bacteria isolated and 26.1% of all bacterial isolates. Other members of Enterobacteriaceae family were also isolated from patients enrolled in this study, such as Citrobacter freundii, which constituted the same incidence rate as K. pneumoniae. Concerning antimicrobial resistance, 11, 10, 9, and 8 out of 12 of E. coli isolates were resistant to Erythromycin, Vancomycin, Tetracycline, and Ceftazidime together, respectively, with a range of resistance from 91.7% to 66.7%. Low percentages of bacteria showed intermediate sensitivity to Imipenem, Gentamicin, Chloramphenicol, Vancomycin, and Erythromycin. However, 12, 11, 10, 10, 9, and 8 out of 12 isolates were susceptible (susceptibility ranged from 100% to 66.7%) to each of Cefotaxime, Chloramphenicol, Imipenem, Amikacin, Ciprofloxacin, and Gentamicin. Conclusions: Escherichia coli was the most common bacteria isolated from human

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UTIs. All of the isolates were multi-drug resistant toward at least four antimicrobials. Particularly, Erythromycin and Vancomycin had no effect on the enteric bacteria at all. Imipenem might be the most effective drug against a large number of the human isolates.

Keywords: Enterobacteriaceae, urinary tract infections, antimicrobial resistance.

Introduction

Infectious diseases constitute one of the most significant difficulties within human communities all over the world. Urinary tract infections (UTIs), among a wide range of microbial infections, are of a double-edged worry with health-care and economic implications (Jahandeh et al., 2016). They are serious diseases that can influence various parts of the urinary tract (Behzadi, 2016).

Approximately, seven million individuals are expected to visit clinics and hospitals due to UTIs per year at an expenditure of over one billion dollars (Gradwohl et al., 2016). Microbial invasion for any portion of the urinary tract, which includes the urethra, bladder, ureters, and kidneys, is referred to as a UTI (Mahdi et al., 2020). Infection of the urinary tract refers to the existence of bacteria in the urine, as well as symptoms and often signs of inflammation, such as repeated micturition, dysuria, pyuria, nycturia, fever, suprapubic pain, and hematuria (Liza et al., 2006; Heising, 2010). It is estimated that UTIs can cost over $1 billion per year (Ahmed et al., 2018). Despite the UTIs constitute 1-6% of total medical consultations; these infections are still the most common among the bacterial infections (Foxman, 2003). It has been suggested that their frequency and burden must be higher than available data because they are not among mandatory diseases to be notified (Öztürk et al., 2020). Women usually have a higher incidence of this infection and are more vulnerable to it due to numerous risk factors leading to infection of up to 2/3 of women with UTIs at some period during their lifetimes (Valiquette, 2001; john et al., 2016). Up to 40% of women will develop UTIs at least once during their lives, and a significant number of these women will have recurrent UTIs (Gradwohl et al., 2016).

Many superimposing factors interact to cause a urinary infection, such as the bacterial inoculum size, the virulence of the infecting bacteria, or factors linked to the host. Inoculation is an early step that results in a UTI, and the most popular hypothesis for inoculation is the ascending route.

Perineum was found to be colonized by enteric bacteria, which then travel up the urethra and bladder (Foxman, 2002). Gram-negative pathogens, mainly from the Enterobacteriaceae family,

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such as Klebsiella pneumoniae, E. coli, Proteus mirabilis, and Enterobacter species, cause the majority of UTIs (Wilson and Gaido, 2004; Griebling, 2005; Foxman, 2010).

Resistance of invasive microorganisms to treatment is still a major global obstacle; this health problem can annually kill thousands of people (Jim, 2014). It is attributed to increased and sometimes uncontrolled antimicrobial use in clinical and agricultural settings (Woolhouse et al., 2015; Hassell et al., 2019). Antimicrobial resistance refers to a microorganism's ability to tolerate their effects and grow in the presence of a chemical that would otherwise inhibit its growth or destroy it (Prestinaci et al., 2015). The rates of resistance to the most commonly prescribed medications for the treatment of UTIs vary greatly across the globe (Farajnia et al., 2009). Furthermore, antibiotic resistance is a major problem that hospital workers must deal with (Edelsberg et al., 2014). Therefore, the current study aimed at characterization of the enteric bacteria isolated from urine of human UTIs and studying their antimicrobial sensitivity.

Materials and methods Ethics

Permission from the hospital authority and signed informed consent from the patients were collected.

All human specimens were handled anonymously based on the ethical and legal standards.

Samples collection

Fifty human urine samples were collected into sterile containers from patients already diagnosed by specialist physicians to have urinary tract infections (UTIs). The patients’ ages ranged from 10 to 60 years and from both genders. All of the urine samples were collected from patients who had not taken any medications that interfere with the results. The samples were gathered from Babylon city, Iraq, from private medical laboratories during 2020.

Bacterial isolation and identification

For routine bacteriological diagnosis, firstly, the urine samples were examined in the laboratory by using dipstick and under the microscope to look for the presence of pus and epithelial cells (inflammatory cells) as an indicator of possible infection. Then, a loopful of the urine sample was streaked onto MacConkey’s agar, which was incubated aerobically at 37ºC for 24-48 hr. Afterwards,

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the plates were inspected for presence of bacterial growth, and the grown colonies were characterized in terms of their features on MacConkey’s agars. The isolates were also identified based on their Gram’s reaction. Subsequently, pure Gram-negative colonies were applied for the biochemical tests including: catalase, oxidase, SIM (sulfide indole motility), sugar fermentation on TSI (triple sugar iron), urease production, indole formation, gelatin liquefaction, citrate utilization, methyl red and Voges-Proskauer tests. All of the isolates were confirmed by using the automated Vitek2 system (bio- Merieux SA, France) according to the manufacturer’s instructions.

Antimicrobial susceptibility tests

Disk diffusion susceptibility method was performed as described by Performance Standards for Antimicrobial Susceptibility Testing (CLSI). Ten different antimicrobial agents were used involving:

Imipenem, Tetracycline, Gentamicin, Chloramphenicol, Amikacin, Ciprofloxacin, Vancomycin, Cefotaxime, Ceftazidime, and Erythromycin.

Results

Identification of the bacterial isolates

The most common bacterium isolated from human urine collected in this study was E. coli, which constituted approximately 85.7% of the enteric bacteria isolated and 26.1% of all bacterial isolates.

Other members of Enterobacteriaceae family were also isolated from the patients enrolled in this study, such as Citrobacter freundii, which constituted the same incidence rate as K. pneumoniae. All of the samples were detected by the traditional biochemical test and confirmed by the Vitek2 system.

Antimicrobial Susceptibility tests

There were 11, 10, 9, and 8 out of 12 E. coli isolates resistant to Erythromycin, Vancomycin, Tetracycline, and Ceftazidime, respectively, with a range of resistance from 91.7% to 66.7%.

However, 12, 11, 10, 10, 9, and 8 out of 12 isolates were susceptible to each of Cefotaxime, Chloramphenicol, Imipenem, Amikacin, Ciprofloxacin, and Gentamicin, respectively (Figure 1).

Additionally, K. pneumoniae isolate showed multi-drug resistance to five antimicrobials including:

Amikacin, Erythromycin, Vancomycin, Cefotaxime, and Ceftazidime (100% resistance).

Furthermore, the isolate revealed 100% intermediate sensitivity to each of Imipenem and Chloramphenicol. However, Tetracycline, Gentamicin, and Ciprofloxacin were more effective

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against the isolate (100% susceptibility) (Figure 2). Interestingly, C. freundii was 100% resistant to all antimicrobials tested, and no susceptibility at all was reported to any drug (Figure 3). Table 1 and table 2 reveals the antimicrobial sensitivity findings of all the enteric bacteria isolated.

Table 1. Antimicrobial susceptibility of the E.coli isolates Antimicrobial

agent

E.coli (N =12)

R (%) I (%) S (%)

Imipenem 1 (8.3) 1 (8.3) 10 (83.3) Tetracycline 9 (75) 0 3 (25) Gentamicin 2 (16.6) 2 (16.6) 8 (66.6) Chlorampheni

col

0 1(8.3) 11 (91.6) Amikacin 2 (16.6) 0 10 (83.3) Ciprofloxacin 3 (25) 0 9 (75) Vancomycin 10 (83.3) 2 (16.6) 0

Cefotaxime 0 0 12 (100)

Ceftazidime 8(66.6) 0 4(33.3) Erythromycin 11(91.9) 1(8.3) 0 R: Resistant, I: Intermediate, S: Susceptible

Table 2 Antimicrobial susceptibility of the klebsiella pneumonia and Citrobacter isolates Antimicrobial

agent

pneumonia (N =1) Citrobacter. F

R (%) I (%) S (%) R(%)

Imipenem 0 1 (100) 0 100

Tetracycline 0 0 1 (100) 100

Gentamicin 0 0 1 (100) 100

Chloramphenicol 0 1 (100) 0 100

Amikacin 1 (100) 0 0 100

Ciprofloxacin 0 0 1 (100) 100

Erythromycin 1 (100) 0 0 100

Vancomycin 1 (100) 0 0 100

Cefotaxime 1 (100) 0 0 100

Ceftazidime 1 (100) 0 0 100

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Figure 1: Disk diffusion antimicrobial susceptibility test for an E. coli isolate tested against 10 antimicrobials.

Figure 2: Disk diffusion antimicrobial susceptibility test shows K. pneumoniae isolate tested against 10 antimicrobials.

Figure 3: Disk diffusion antimicrobial susceptibility test shows multidrug resistant C. freundii tested against 10 antimicrobials.

Discussion

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Urinary tract infection (UTI) is one of the most prevalent diseases with diverse etiological agents. It is common in most regions of Iraq and remains a major health problem in many developing countries (Troeger et al., 2017). In the current study, the ratio of female patients with UTI was more than that of males, this is consistent with other researchers (Hadi et al., 2014; Ahmed et al., 2019;

Mahdi et al ., 2020). However, in other studies, no significant difference was observed between bacterial infections of female and male urinary system infections (Normohammadzadeh et al., 2003; Hajikolaei et al., 2015). By contrast to the present study, statistically significant prevalence of UTI was noticed in male more than female (Fatihu and Addo, 1991).

The most common bacterium isolated from human urine collected in this study was E. coli, which constituted approximately 85.7% of the enteric bacteria isolated and 26.1% of all bacterial isolates. This result is in agreement with other studies (Faisal et al., 2013; Hussein et al., 2017;

Abdulrahman and Salih, 2018; Ghaima et al., 2018; Mahdi et al., 2020), in which these studies were performed in different regions in Iraq, and found that E. coli was the major causative agent of UTI in Iraq. In addition, it is known that the same organism was reported to be the major cause of UTI worldwide (Córdoba et al., 2017; Holguin and Fernandez, 2019). However, other authors reported very low isolation rate of E. coli, and the most prevalent Gram-negative pathogens were Klebsiella spp. (Ngwai et al., 2010; Hammoudi and Atyia, 2013). In contrast, the current study revealed very low incidence rate (2.17%) of K. pneumoniae among other isolates.

Other members of Enterobacteriaceae family were also isolated from UTIs of patients enrolled in this study, such as C. freundii, which constituted the same incidence rate as K.

pneumoniae. It has been found that C. freundii is the third most common organism causing UTI in hospitalized patients after E. coli and Klebsiella species (Metri et al., 2013; Salih et al., 2016).

In comparison with other studies, E. coli was also found to be resistant to Ceftazidime, Erythromycin and Tetracycline (Kazemnia et al., 2014; Hussein et al., 2017; Jahani et al., 2017).

However, the isolates of this bacterium were 100% sensitive to Ceftazidime in the study of Yassin et al., (2017). Regarding Imipenem and Cefotaxime, their findings in the current study are similar

to other reports, including that of Ghaima et al., (2018) in Baghdad, Hadi et al., (2014) in Basra, and another international study of Dromigny et al., (2005). Concerning K. Pneumoniae isolated in this study, it showed Erythromycin resistance, this is consistent with other studies (Ogunshe et al., 2010; Osman et al., 2014). While resistance of the current isolate to Ceftazidime converses Hakonsholm et al., (2020) who noticed no inhibitory effect by Ceftazidime, it coincides with

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Kareem and Rasheed (2011). Similarly, another study performed in Baghdad showed 100%

resistance to Cefotaxime (Ahmed et al., 2020). The sensitivity of the isolate to Gentamicin and Tetracycline was confirmed by other studies (Kazemnia et al., 2014; Chaudhary et al., 2020).

Nevertheless, other studies carried out in Iraq showed resistance of K. pneumoniae in particular to Tetracycline (Khalaf and Al-Hasso, 2005; Hammoudi and Atyia, 2013).

Furthermore, C. freundii, was resistant (100%) to all antimicrobials tested, and no susceptibility at all was reported to any drug. This bacterium was also found, in a study done in China, to be resistant to multiple antibacterial agents (Li et al., 2018). Likewise, another study performed in Al- Najaf city, Iraq, 50% of C. freundii isolated from UTI patients demonstrated extensive-drug resistance (Tuwaij, 2016).

Conclusion

Escherichia coli was the most common bacteria isolated from human urinary tract infections.

Approximately, all E. coli isolates showed a degree of similarity in their antimicrobial susceptibly profile. All of the isolates of this study were multi-drug resistant toward at least four antimicrobials.

Particularly, Erythromycin and Vancomycin had no effect on the enteric bacteria at all. On the other hand, Imipenem might be the most effective drug against a large number of the isolates.

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