Proceeding Paper

Epidemiological study of antimicrobial resistance pattern of

suspected urinary tract infection in a super surgical, super spe-
cialty hospital in Northern India
Narayan Ahirwar 1,2, Tapan Kumar Singha 3*, Malvika Srivastava 1 and Manisha Pal 3

1. Department of Microbiology and Serology, Sanar International Hospitals, Gurgaon, India.

2. Department of Microbiology, Sunrise University, Alwar, Rajasthan, India.
3. Department of Microbiology, MolQ Laboratory, Gurugram, Haryana, India.
* Correspondence: Email Id: tapanmicro123@[Link], Phone No.: +91-7206287339

Abstract: Background: This study aimed to assess the antimicrobial resistance profiles of urinary
tract infection (UTI) collected from individuals of various age groups, both male and female. Meth-
ods: This study analyzed 266 urine samples from diverse individuals. Midstream urine samples
were collected, transported, and processed on CLED medium within two hours. Bacterial identifi-
cation was done based on colony morphology, Gram staining, and biochemical characteristics. The
VITEK 2 Compact system (Biomerieux, France) was used for antimicrobial susceptibility testing,
ESBL detection, and Carbapenemase detection. Results: Out of 61 significant UTIs in both male and
female patients, 78.69% were caused by gram-negative bacteria, 11.48% by gram-positive bacteria,
and 9.84% by Candida species. Escherichia coli (37.70%), Klebsiella pneumoniae (26.22%), and Pseudo-
monas aeruginosa (11.47%) were the most common uropathogens. Tetracycline (88.89%) and ceftriax-
one (77.14%) showed high resistance, while amikacin (89.36%) and colistin (97.30%) were the most
effective against both gram-negative and gram-positive uropathogens. Colistin susceptibility was
exclusively observed in cases of multidrug resistance (MDR) and pandrug resistance (PDR). Con-
clusions: This study indicates that gram-negative bacteria, particularly E. coli, are responsible for a
higher number of UTIs compared to gram-positive uropathogens. Amikacin and colistin were iden-
tified as the most effective antibiotics against both gram-negative and gram-positive uropathogens.
Citation: Ahirwar, N.; Singha, T.K.;
Srivastava, M.; Pal, M. Epidemiolog- Keywords: Urinary tract infection; uropathogens; antibiotic susceptibility; antimicrobial resistance;
ical study of antimicrobial resistance
gram-positive bacteria; gram-negative bacteria
pattern of suspected urinary tract in-
fection in a super surgical, super
specialty hospital in Northern India.
2023, volume number, x.
[Link]
1. Background
Urinary tract infections (UTIs) are incredibly prevalent, affecting people of all ages
Academic Editor(s): Name
and genders worldwide, with millions of cases reported annually [1]. Among UTI cases,
Published: date Escherichia coli stands out as the leading cause, responsible for approximately 90% of
community-reported cases and 50% of hospital-reported cases [2,3]. In addition to E. coli,
various other pathogens, such as Klebsiella species, Proteus species, Acinetobacter species,
Copyright: © 2023 by the authors. Pseudomonas species, Staphylococcus species, Enterococcus species, and Streptococcus spe-
Submitted for possible open access cies, are also identified as uropathogens [4,5]. Frequent UTI symptoms that patients com-
publication under the terms and monly encounter include dysuria, polyuria, and cystitis [6]. Failing to address UTIs can
conditions of the Creative Commons result in severe health complications, including kidney damage, renal scarring, and renal
Attribution (CC BY) license failure [7]. This issue affects a significant portion of adult females, with approximately 40-
([Link] 50% experiencing UTIs [6]. The increased incidence of UTIs in adult females can be at-
s/by/4.0/). tributed to factors like sexual activity and pregnancy [8]. In women, the prevalence of
UTIs tends to rise by 5% over a decade, while the occurrence of UTIs during pregnancy
sees an approximate 7% increase [6]. In males, the frequency of UTI cases tends to rise
with age, often due to declining immunity. Additionally, common factors contributing to
UTIs in males encompass issues like urethral structure, bladder neck obstructions, bladder
stones, bladder tumors, bladder diverticula, enlarged prostate gland and prostate cancer
[9].
UTIs are also relatively common in children and infants under the age of approxi-
mately 2 years, and can be acquired both in community settings and hospitals [10]. Up to
the age of 7 years, approximately 5% of girls and 2% of boy’s experience at least one UTI
incident [11,12]. Diagnosing UTIs in younger children can be challenging, as they may be
unable to articulate their symptoms. Conversely, older children may express urinary dis-
comfort, including a burning sensation during urination, loss of bladder control, increased
urination frequency, and malodorous urine, among other complaints [13]. Notably, a
higher number of complicated UTI cases are observed in males, while uncomplicated UTIs
are typically treated without the need for culture testing and sensitivity analysis [14]. In
many instances, UTIs are often characterized as re-infections because the condition re-
emerges after several weeks of antibiotic treatment. The primary instigator of these infec-
tions is the initial bacterial attachment, which subsequently leads to the formation of a
biofilm, offering resistance against the host's immune responses [15]. Numerous studies
have reported multiple antimicrobial resistances among uropathogens, with concerns es-
calating globally, particularly regarding multidrug resistance (MDR) and extended-spec-
trum beta-lactamases (ESBLs) [6,15].
Consequently, effective management of urinary tract infections and the establish-
ment of antibiotic guidelines are of paramount importance in combatting antibiotic re-
sistance and multidrug resistance. In this context, clinical microbiologists play a crucial
role in identifying pathogenic organisms and collaborating with physicians to develop
personalized antibiotic therapies for each patient, thus reducing the inappropriate use of
antibiotics, dosing errors, and potential drug interactions. Ultimately, this approach en-
hances the quality of care provided to patients. Therefore, the primary goal of this study
is to assess the antimicrobial susceptibility patterns in positive UTI samples isolated from
both male and female patients.

2. Methods
2.1. Study Population
The study took place from January to July 2023 at the Microbiology Department of
Sanar International Hospitals in Gurgaon, India. 266 samples were collected from diverse
urine samples, with 161 from male patients and 105 from female patients, both from the
outpatient and inpatient departments.

2.2. Sample Collection

Clean-catch midstream urine (MSU) samples were collected from suspected UTI pa-
tients using 20 ml sterile screw-capped containers (BD Urine Collection Kit). To prevent
bacterial growth, samples were transferred to a container where boric acid was added (0.2
mg). Aseptic sample collection instruction was provided to patients for proper urethral
sample collection [16].

2.3. Sample Processing

A 4 mm nichrome wire inoculating loop was used to inoculate urine samples on Cys-
teine lactose electrolyte deficient (CLED) agar medium, with an inoculum size of 0.01 ml.
The culture plates were then incubated at 37℃ for 24 to 48 hours. After incubation, plates
were checked for clear, distinct bacterial growth. If no colonies were visible, the incubation
extended by 24 hours. To confirm positive urine cultures, we relied on colony counts ex-
ceeding >103 to 105 CFU/ml, indicating significant bacteriuria.
2.4. Identification and Sensitivity
Positive bacterial isolates were identified by their colony morphology, Gram stain-
ing, and biochemical characteristics. Gram-negative isolates were identified using the VI-
TEK 2 Compact machine with the GN ID-card, while Gram-positive isolates and yeast-
like cells like Candida were identified using GP ID-card and YST ID-card in the VITEK 2
Compact machine, respectively.
Antimicrobial susceptibility testing was conducted using the widely recognized VI-
TEK 2 Compact system. To maintain consistency, we prepared a McFarland standard in-
oculum with an OD of 0.5, which was assessed with a Vitek Densicheck display base ma-
chine (Ref. No- 422220) following established standards. The testing procedure followed
the guidelines established by the Clinical and Laboratory Standards Institute (CLSI) in
2022. Vitek cards were used for antimicrobial susceptibility testing, including AST-N405,
AST-406, and AST-407 for gram-negative bacteria, AST-P628 for gram-positive bacteria,
and AST-YS08 for Candida. The VITEK 2 Compact system was used to detect ESBL pro-
duction, which was confirmed through a synergistic assay between AMC and a 3rd or 4th
generation cephalosporin.

3. Results
Over a span of 7 months, 266 urine samples from individuals suspected of urinary
tract infections (UTIs) were investigated. Among these samples, 161 (60.53%) were from
male patients, and 105 (39.47%) were from female patients. The analysis revealed 61
(22.93%) significant UTI cases in both male and female patients. When examining positive
bacterial isolates, a higher occurrence was observed in female patients, with 34 (55.74%)
cases, compared to 27 (44.26%) in male patients. The positive isolates were categorized
into four age groups: 1-16, 17-35, 36-60, and over 60 years. The percentage of UTI occur-
rence in female samples was highest (83.33%) in the 1-16 age group and lowest (37.50%)
in the 36-60 age group, indicating a decrease in UTI occurrence with increasing age. Con-
versely, for male-positive samples, the UTI occurrence was highest (62.50%) in the 36-60
age group and lowest (16.67%) in the 1-16 age group. This suggests that the trend of UTI
occurrence in male samples generally increased with age, except for the 1-16 age group,
but decreased in the over 60 age group (29.41%). A total of 61 uropathogenic microorgan-
isms were identified, comprising 48 (78.69%) gram-negative bacteria, 7 (11.48%) gram-
positive bacteria, and 6 (9.84%) Candida species. Among the isolated uropathogens, Esch-
erichia coli emerged as the most prevalent, accounting for 37.70% of the cases. The second
most frequently isolated microorganism was Klebsiella pneumoniae (26.22%), followed by
Pseudomonas aeruginosa (11.47%), Enterococcus faecalis (4.91%), Candida albicans (4.91%),
Candida tropicalis (4.91%), Citrobacter koseri (3.27%), Staphylococcus haemolyticus (3.27%), En-
terococcus gallinarum (1.63%), and Staphylococcus hominis (1.63%), as illustrated in Figure 1.
The antibiotic susceptibility results revealed that tetracycline displayed the highest
resistance (88.89%) among all the uropathogens, followed by ceftriaxone (77.14%). Con-
versely, colistin (97.30%) and amikacin (89.36%) exhibited the highest sensitivity for both
groups. Detailed antibiotic susceptibility data are presented in Figure 2.
Escherichia coli exhibited remarkable resistance to ceftazidime (75.00%) and ciproflox-
acin (73.91%), while it displayed its highest sensitivity to tigecycline, colistin, and nitrofu-
rantoin (100.00%) (Figure 3). In the case of Klebsiella pneumoniae, resistance was prevalent
against ceftazidime (100.00%) and cefuroxime (83.33%), but susceptibility was observed
towards amikacin (93.33%), colistin (92.86%), and fosfomycin (71.43%). Pseudomonas aeru-
ginosa, on the other hand, showed a high susceptibility to nitrofurantoin, colistin, and az-
treonam (100.00%), but proved resistant to ceftazidime and levofloxacin (60.00%) (Figure
3). Enterococcus faecalis exhibited an extensive resistance to tetracycline (100.00%), but com-
plete susceptibility to nitrofurantoin, vancomycin, and linezolid (100.00%) (Figure 3).
 Notably, Candida albicans and Candida tropicalis demonstrated complete sensitivity to
all tested antibiotics (amphotericin B, caspofungin, flucytosine, fluconazole, micafungin,
vancomycin).
In terms of resistance mechanisms, 30.43% of Escherichia coli and 18.75% of Klebsiella
pneumoniae among the total isolates were extended spectrum β-lactamase producers. Ad-
ditionally, 17.39% of Escherichia coli and 56.25% of Klebsiella pneumoniae were identified as
carbapenemase producers.

Figure 1. Occurrence of positive organisms in urine samples.

Figure 2. Overall, antibiotic susceptibility pattern observed in positive urine samples.
Figure 3. Antibiotic resistance pattern against organisms.
 4. Discussion 1
The investigation aimed to assess the rising trend of antimicrobial resistance among 2
uropathogens and enhance effective treatment strategies. Antimicrobial resistance has 3
been on the rise globally over time [17]. In our study, the overall UTI occurrence was 4
22.93%, with some studies reporting lower (e.g., 13.9%, 17%, 17.26%) and others reporting 5
higher (e.g., 23.7%, 32.7%, 53.82%) rates [17–22]. We observed a higher UTI occurrence in 6
females (55.74%) compared to males (44.26%), consistent with other studies [23,24]. 7
Among males, UTI cases increased with age, possibly due to weakened immunity, pros- 8
tate issues, or prostate enlargement [11,17]. The age-wise distribution of susceptible UTI 9
patients in females ranged from >60 years (35.29%), 17-35 years (32.35%), 36-60 years 10
(17.64%), to 1-16 years (14.70%). For males, the distribution was 17-35 years (40.74%), 36- 11
60 years (37.03%), >60 years (18.51%), and 1-16 years (3.70%). In Ethiopia, a similar study 12
found the highest UTI prevalence in the >45 age group (23.4%), while a Ugandan study 13
reported the highest occurrence in the 20-29 age group (32.6), differing from our findings 14
[25,26]. Another study in 2021 reported the highest frequency in the 21-30 age group 15
(22.8%) [27]. We found a 78.69% occurrence of gram-negative bacteria and 11.48% of 16
gram-positive bacterial isolates, differing from other studies [28,29]. Escherichia coli was 17
the predominant uropathogen (37.70%), followed by Klebsiella pneumoniae (26.22%), and 18
Pseudomonas aeruginosa (11.47%) (Figure 1). While previous research has explored the 19
prevalence of E. coli as a uropathogen and reported higher rates, such as 50.09% [30], 50% 20
[28], and 42.7% [21], it's important to note that E. coli and K. pneumoniae collectively account 21
for over 80% of UTI cases globally, occurring in both community and hospital-acquired 22
infections [31,32]. Tetracycline exhibited the highest resistance (88.89%), while colistin 23
showed the highest sensitivity (97.30%) [14,33,34]. Notably, the treatment of uncompli- 24
cated UTIs without culture and susceptibility reports has contributed to increased antimi- 25
crobial resistance [35]. Among Escherichia coli isolates, 75.00% were resistant to 26
ceftazidime, while nitrofurantoin, tigecycline, and colistin were highly effective (100.00%). 27
In a study conducted in Northeast Ethiopia by Adugna and collaborators, they also found 28
that tetracycline exhibited the highest resistance rate at 65.70%, while colistin was identi- 29
fied as the most effective drug with a 100.00% success rate against E. coli [21]. Klebsiella 30
pneumoniae showed 100.00% resistance to ceftazidime but high sensitivity to Amikacin 31
(93.33%), colistin (92.86%), and fosfomycin (71.43%) which is comparable to other studies 32
also [36,37]. Pseudomonas aeruginosa was highly resistant to ceftazidime and levofloxacin 33
(60.00%) but sensitive to nitrofurantoin, colistin, and aztreonam (100.00%). Linezolid and 34
nitrofurantoin (100.0%) were effective against enterococcus faecalis, while tetracycline ex- 35
hibited 100.00% resistance. 36
The majority of organisms showed resistance specially to the beta-lactam antibiotics, 37
but on the other hand, recent drugs like amikacin, colistin, nitrofurantoin, and fosfomycin 38
proved effective in fighting uropathogens. 39

5. Conclusion 40
Our findings reveal a captivating picture of urinary tract infections, where Gram- 41
negative organisms, with E. coli at the forefront, take center stage as the most prevalent 42
culprits. In the dynamic landscape of antibiotic susceptibility, tetracycline consistently 43
presents a formidable opponent, while on the opposite end of the spectrum, colistin and 44
amikacin emerge as the champions, demonstrating their unparalleled effectiveness. The 45
escalating challenge of antimicrobial resistance finds its roots in various factors, including 46
the intricate battle against UTIs in cancer patients and the complexities of treating intricate 47
urinary tract infections. Equally noteworthy is the practice of addressing uncomplicated 48
UTIs without the invaluable guidance of culture and susceptibility reports, inadvertently 49
contributing to the formidable rise in resistance. Delving deeper, a constellation of risk 50
factors comes into play, with patient age, gender, diabetes, catheter use, immune 51

Antibiotics 2023, 12, x. [Link] [Link]/journal/antibiotics

Antibiotics 2023, 12, x FOR PEER REVIEW 2 of 9

compromise, and prior antibiotic history all influencing the heightened susceptibility to 52
urinary tract infections. Amid this intricate tapestry of factors, bacteriological culture 53
stands as a beacon of diagnostic significance. It not only confirms the presence of infec- 54
tions but also plays a pivotal role in the crucial identification of the responsible microor- 55
ganisms. 56

Author’s contributions: Narayan Ahirwar: Conceptualization, Methodology, data collection and 57

analysis, Writing - original draft. Tapan Kumar Singha: Conceptualization, Supervision, review, and 58
editing. Malvika Srivastava: Conceptualization, manuscript editing, and critical review. Manisha 59
Pal: Data acquisition and analysis. 60

Funding: This research received no external funding. 61

Institutional Review Board Statement: The present study protocol was reviewed and approved by 62
Medical Superintendent, Sanar International Hospitals Gurugram (Ref. No: SIH010622/SR01) Con- 63
sent for inclusion of the samples for the study was taken by the patients at the time of sample col- 64
lection. 65

Informed Consent Statement: Informed consent was obtained from all subjects involved in the 66
study. 67

Data Availability statement: The datasets used and/or analysed during the current study are avail- 68
able from the corresponding author on reasonable request. 69

Acknowledgments: The authors are highly thankful to Sanar International Hospitals for providing 70
infrastructures and support to carry out this study successfully. 71

Conflicts of Interest: The authors declare no conflict of interest. 72

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