Get Permission Gahlot, Netam, Dadarya, Sherwani, and Gaur: Epidemiology, microbiological profile and susceptibility pattern of uropathogens from a tertiary care hospital in central India


Introduction

Urinary tract infections (UTIs) are the most prevalent bacterial infections seen in clinical settings, and its presentations range from asymptomatic bacteriuria to severe sepsis.1 It poses a significant healthcare burden, as it is one of the leading causes of hospital visits, contributing substantially to morbidity as well. It was estimated that there were 404.61 million cases of UTIs globally in 2019, resulting in 236,790 deaths and 520,200 disability-adjusted life years (DALYs).2 UTIs accounted for 75% of hospital-acquired infections among patients admitted to a urology ward as indicated by a study conducted in India.3 The high incidence of UTIs burdens the healthcare systems and individuals leading to increased healthcare costs and greater antibiotic consumption, which can promote antimicrobial resistance.4

Gram-negative bacteria, particularly Escherichia coli (uropathogenic), are the predominant uropathogens responsible for UTIs. Other common urinary pathogens include Klebsiella species, Proteus species, Staphylococcus aureus, Enterobacter species, Citrobacter species, Pseudomonas aeruginosa, Acinetobacter species, Enterococcus species, and Candida albicans.5 The isolation of multidrug-resistant organisms is common, especially among patients using urinary catheters in the upper urinary tract or with prior urinary tract infections. 6

To reduce the emergence of resistance and optimize the treatment outcomes targeted antibiotics based on susceptibility testing are essential. 7 The distribution of uropathogens and their susceptibility patterns can differ significantly across regions, making the generation of local antimicrobial resistance data vital for guiding empirical treatment and developing stewardship programs.8

This study aimed to characterize the epidemiology, microbiological profile, and antimicrobial susceptibility patterns of uropathogens isolated from patients at a tertiary care hospital in Chhattisgarh state, central India, and contribute data that could be valuable for formulating healthcare policies at local, national, and global levels.

Materials and Methods

This retrospective descriptive study was conducted in the Department of Microbiology at Pt. Jawahar Lal Memorial Medical College in Raipur, Chhattisgarh, India, from January 2022 to December 2022. During this period, 2,893 urine samples were collected from patients in both inpatient and outpatient departments of Dr. BR Ambedkar Memorial Hospital, Raipur, following standard sample collection protocols. Only the first isolate from each patient was included, and duplicate samples were excluded. The urine samples were processed for colony counts using a semi-quantitative method on cystine lactose electrolyte-deficient (CLED) agar medium with calibrated loops, according to standard protocols. Susceptibility testing was performed using the Kirby-Bauer disk diffusion method and interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guidelines in the M100 document, 32nd edition. Data on age, gender, location (OPD/IPD), and other demographic factors of the positive cases were recorded. As this study is retrospective, the data were collected from records in the microbiology department and analyzed further.

Sample collection

As per the patient's condition, either midstream clean catch urine or urine from Foley’s catheter was collected and transported to the lab within 2 hours for further processing following standard microbiological protocols. In case of delay, the specimen was stored in the refrigerator for not more than 24 hours.9

Culture

Each specimen was cultured on Cystine Lactose Electrolyte Deficient (CLED) Agar using the semi-quantitative Calibrated Loop/Surface Streak Method. Plates were incubated aerobically at 35–37°C for 18–24 hours. Specimens showing significant growth, with bacteria growing >104 colony-forming units (CFU/mL) with a single morphotype or up to 2 types, were considered significant and processed further for identification and susceptibility testing. Specimens belonging to patients with signs of systemic infection or recurrent urinary tract infections were also considered significant and processed if a single pure-growth organism was isolated even when the colony counts were <104CFU/mL.10

Identification

The isolated organisms were identified through conventional methods by observing biochemical reactions as per standard microbiological practices.11

Antimicrobial susceptibility testing

It was conducted using the Kirby-Bauer disc diffusion method as per CLSI M-100 guidelines (32nd edition). Antibiotic susceptibility of the isolates was tested on Mueller-Hinton agar plates, with results interpreted after incubation at 37°C for 24 hours by measuring the zone of inhibition.12

Ethical statement

The study received approval from the Institutional Ethics Committee of Pt. J.N.M. Medical College, Raipur, on 28-03-2022. All procedures adhered to the ethical standards of the 2008 Declaration of Helsinki.

Statistical analyses

These were performed using SPSS Statistics version 27.0 (IBM Corp., Armonk, NY, USA), WHONET, and Microsoft Excel. Data were presented in the form of tables, charts, and graphs to comprehensively elucidate the findings.

Results

Total number of urine samples received from suspected UTI cases was 2893 out of which 1719 samples were from inpatients and 1174 samples were from outpatients. Out of 2893 samples, 784 showed significant growth on culture, 602 showed insignificant bacteriuria and 1507 showed no growth.

Patient demography

Females were more affected (70.28%) than males (29.72%), thus giving female to male (F: M) ratio as2.3:1. Among females most common age group affected was 21-40 years (36.73%) while in males most common age group affected was 41-60 years. (Table 1).

Location wise distribution

A maximum number of samples that showed significant growth belonged to the Department of Gynaecology & Obstetrics (32.65%) followed by the Department of Medicine (32.02%).(Table 2)

Microbiological profile

Most common causative organism found in this study was Escherichia coli (41.9%) followed by Enterococcus species (23.98%). Significant growth of Candida species was found in 13.3%of samples out of which only 2.29% were of Candida albicans remaining were non-albicans. (Table 3)

Antimicrobial susceptibility pattern

Gram-negative isolates

Among the Gram-negative fermenter group, Escherichia coli isolates showed 100% susceptibility to fosfomycin; for nitrofurantoin, the susceptibility was 93% while for carbapenems it was 96%.

In the case of isolates of Klebsiella pneumonia, the susceptibility percentage for carbapenems, fluoroquinolones, and nitrofurantoin were 82%, 72%, and 59% respectively. (Table 4)

Among the Gram-negative non-fermenter group, Acinetobacter baumanniii isolates were most susceptible to meropenem (68%) and piperacillin-tazobactam (62%).

Isolates of Pseudomonas aeruginosa showed maximum susceptibility to gentamicin (92%), netilmicin (89%), and piperacillin-tazobactam (87%). (Table 4)

Gram-positive isolates

In Enterococcus species isolates, no resistance was seen against teicoplanin and Fosfomycin, 82% were susceptible to Nitrofurantoin, 97% were susceptible to linezolid and 94% were susceptible to Vancomycin. Among the 12 isolates of Staphylococcus aureus, 8 were methicillin-resistant Staphylococcus aureus (MRSA). (Table 5)

Table 1

Distribution of UTI cases according to age & gender

Age (in years)

Male

Female

0-20

58 (7.40%)

81(10.33%)

21-40

58(7.40%)

288(36.73%)

41-60

65 (8.29%)

127(16.20%)

61-80

49 (6.25%)

50(6.38%)

81 Above

3 (0.38%)

5(0.64%)

Total

233

551

[i] Male to Female Ratio (M:F) = 1:2.3

Table 2

Distribution of UTI cases according to location

Name of Department

Number of cases

Gynaecology & obstetrics

256 (32.65%)

Oncology

14(1.79%)

Dermatology

3(0.38%)

ENT

2(0.26%)

ICU

54(6.89%)

Medicine

251(32.02%)

OPD

26(3.32%)

Orthopedics

16(2.04%)

Paediatrics

68(8.67%)

Surgery

94(11.99%)

Total

784

Table 3

Microbiological profile of UTI cases

Organisms isolated

Gram Negative (Fermenters)

Escherichia coli

329 (41.96%)

Klebsiella pneumoniae

81(10.33%)

Citrobacter species

3(0.38%)

Proteus species

5(0.63%)

Gram Negative (Non-Fermenters)

Acinetobacter baumannii

23(2.93%)

Pseudomonas aeruginosa

38(4.85%)

Gram positive cocci

Enterococcus species

188(23.98%)

Staphylococcus aureus

12(1.53%)

Yeasts

Candida albicans

18(2.29%)

Non-albicans Candida

87(11.09%)

Total

784

Table 4

Antibiogram 1: % susceptibility of gram-negative isolates in urine sample

Antibiogram 1; Gram Negative bacilli in Urine Sample

Escherichia coli

Klebsiella pneumoniae

Acinetobacter baumannii

Pseudomonas aeroginosa

Number of Isolates

329

81

23

19

Ampicillin

16%

R

R

R

Ampicillin/Sulbactam

60%

48%

50%

-

Amoxicillin-clavulanate

59%

49%

R

R

Piperacillin/Tazobactum

64%

55%

62%

87%

Cefotaxime

22%

26%

41%

R

Ceftriaxone

24%

36%

41%

R

Ceftazidime

31%

45%

53%

82%

Cefepime

43%

50%

60%

79%

Aztreonam

60%

49%

R

R

Cephazolin

15%

30%

R

R

Imipenem

96%

82%

67%

80%

Meropenem

96%

81%

69%

83%

Ciprofloxacin

76%

72%

60%

_

Levofloxacin

71%

71%

67%

66%

Gentamicin

73%

59%

59%

92%

Amikacin

80%

56%

43%

82%

Netilmicin

-

-

-

89%

Tobramycin

-

-

-

57%

Cefuroxime

21%

30%

38%

-

Cefoxitin

36%

42%

38%

R

Nitrofurantoin

93%

59%

48%

-

Cotrimoxazole

50%

46%

61%

R

[i] R-Intrinsically Resistant 1, N-Not to be reported even if susceptible 1, “-“-No breakpoints available

Table 5

Antibiogram 2: % susceptibility of Gram-positive isolates in Urine sample

Antibiogram 2; Gram Positive cocci in Urine Sample

Enterococcus species

Staphylococcus aureus

Number of Isolates

188

4

Ampicillin

78%

-

Penicillin

77%

-

Cefoxitin

R*

33%

Rifampin

R*

100%

Ciprofloxacin

29%

-

Levofloxacin

52%

-

Nitroforantoin

82%

-

Gentamicin

R*

50%

Gentamicin (High level)

68%

Linezolid

97%

100%

Doxycycline

50%

75%

Higl Level Streptomycin

76%

-

Vancomycin

94%

-

Teicoplanin

100%

-

Trimethoprim/Sulfamethoxazole

R*

100%

[i] R-Intrinsically Resistant 1, N-Not to be reported even if susceptible 1, “-“-No breakpoints available

Discussion

A comprehensive understanding of microbial distribution and its resistance patterns is critical for the effective management and treatment of urinary tract infections (UTIs). This study revealed that UTIs were more prevalent among females, corroborating earlier findings that females are at a higher risk due to their shorter urethra and proximity of the urethral opening to the anus. Age-wise, the sexually active females were more affected, possibly due to increased exposure and poor hygiene maintenance. In men, an increase in the incidence was seen at the age between 40-60 years which could be associated with increased urinary retention caused due to benign prostrate hypertrophy in that age group. These results aligned with another study from India.13

Escherichia coli emerged as the predominant pathogen, responsible for the majority of UTIs, followed by Enterococcus species. This pattern is in concurrence with numerous studies globally, indicating that Escherichia coli is the most common uropathogen, accounting for up to 80% of UTIs.14 Notably, there was a substantial prevalence of other uropathogens, such as Klebsiella pneumoniae, Pseudomonas aeruginosa, and Acinetobacter baumannii, indicating a preponderance of Gram-negative bacilli as responsible agents for UTIs in this region as corroborated in another study.15 Although 105 isolates of Candida species with significant growth were found, their clinical implication as uropathogenic is hard to establish.

Antibiotic susceptibility testing revealed that Escherichia coli and Klebsiella pneumoniae exhibited resistance to multiple antibiotics, including ampicillin, cotrimoxazole, and third-generation cephalosporins, a trend increasingly reported worldwide.16, 17 This high level of resistance can be attributed to the irrational use of antibiotics and the lack of proper stewardship. Consequently, this development necessitates a careful selection of empirical therapy, with nitrofurantoin and fosfomycin recommended for uncomplicated UTIs, as supported by similar studies.18, 19

This study had several limitations. Being a retrospective observational study, it is subject to selection bias. Additionally, we were unable to assess or report on potential clinical outcomes such as symptoms, complications, treatment efficacy, and recurrence rates. As it was a retrospective study the data to determine whether the infection was hospital acquired could not be retrieved. The sample collection method, performed either by hospital staff or by patients themselves, introduced variability that was beyond our control. Moreover, errors in the collection, storage, and transport of specimens to the laboratory could not be determined which may have further impacted the study's findings.

Conclusion

In conclusion, this study provides valuable insights into the current status of UTIs in Central India. Escherichia coli remains the most common causative agent followed by Klebsiella pneumoniae. Point of concern was high level of associated multi-drug resistance. Nitrofurantoin emerged to be the choice for empirical therapy. However, future research should adopt a prospective study design to enhance diagnosis and treatment for patients in the region. Escherichia coli remains the principal uropathogen, and the increasing antimicrobial resistance underscores the need for routine surveillance, rational antibiotic use, and effective infection control measures. Efforts should focus on minimizing the spread of resistant bacteria through appropriate infection control, which is a crucial step in addressing the issue of resistant microorganisms.

Source of Funding

None.

Conflict of Interest

The authors declare that there are no conflicts of interest associated with this manuscript.

References

1 

AJ Schaeffer PC Walsh AB Retik ED Vaughan AJ Wein Infections of the Urinary TractCampbell’s Urology8th EdSaundersPhiladelphia2002515602

2 

JD Sleigh MC Timbury Notes on Medical BacteriologyChurchill Livingstone IncNew York19862128

3 

M Turck W Stamm Nosocomial infection of the urinary tractAm J Med19817036514

4 

JAD Neto LDM da Silva ACP Martins RB Tiraboschi ALA Domingos HJ Suaid Prevalence and bacterial susceptibility of hospital acquired urinary tract infectionsActa Cir Bras200318368

5 

G Beyene W Tsegaye Bacterial uropathogens in urinary tract infection and antibiotic susceptibility pattern in jimma university specialized hospital, southwest ethiopiaEthiop J Health Sci20112121416

6 

AF Moges A Genetu G Mengistu Antibiotic sensitivities of common bacterial pathogens in urinary tract infections at Gondar Hospital, EthiopiaEast Afr Med J20027931402

7 

DJ Farrell I Morrissey DD Rubeis M Robbins D Felmingham A UK multicentre study of the antimicrobial susceptibility of bacterial pathogens causing urinary tract infectionJ Infect200346294100

8 

D Mathai RN Jones MA Pfaller Epidemiology and frequency of resistance among pathogens causing urinary tract infections in 1,510 hospitalized patients: a report from the SENTRY Antimicrobial Surveillance Program (North America)Diagn Microbiol Infect Dis200140312936

9 

JG Collee RS Miles B Watt JG Collee AG Fraser BP Marmion A Simmons Laboratory strategy in the diagnosis of infective syndromesMackie & McCartney Practical Medical Microbiology14th EdElsevierNew York1996848

10 

N Karah R Rafei W Elamin A Ghazy A Abbara M Hamze Guideline for Urine Culture and Biochemical Identification of Bacterial Urinary Pathogens in Low-Resource SettingsDiagnostics (Basel)20201010832

11 

JG Collee RS Miles B Watt JG Collee BP Marmion AG Fraser A Simmons Tests for Identification of BacteriaMackie & McCartney Practical Medical Microbiology14th edElsevier PublicationNew York199613151

12 

Clinical and Laboratory Standards Institute Performance standards for antimicrobial disk susceptibility tests. M10032 edClinical and Laboratory Standards InstituteWayne, PA2022

13 

P Pardeshi Prevalence of urinary tract infections and current scenario of antibiotic susceptibility pattern of bacteria causing UTIIndian J Microbiol Res2018533348

14 

AL Flores-Mireles JN Walker M Caparon SJ Hultgren Urinary tract infections: epidemiology, mechanisms of infection and treatment optionsNat Rev Microbiol201513526984

15 

HB Patel ST Soni A Bhagyalaxmi NM Patel Causative agents of urinary tract infections and their antimicrobial susceptibility patterns at a referral center in Western India: An audit to help clinicians prevent antibiotic misuseJ Family Med Prim Care2019811549

16 

P Mehrishi SS Faujdar S Kumar S Solanki A Sharma Antibiotic Susceptibility Profile of Uropathogens in Rural Population of Himachal Pradesh, India Where We are Heading?Biomed Biotechnol Res J2019331715

17 

K Gupta TM Hooton KG Naber B Wullt R Colgan LG Miller International Clinical Practice Guidelines for the Treatment of Acute Uncomplicated Cystitis and Pyelonephritis in Women: A 2010 Update by the Infectious Diseases Society of America and the European Society for Microbiology and Infectious DiseasesClinl Infect Dis201152510320

18 

N Kumar K Chatterjee S Deka R Shankar D Kalita Increased Isolation of Extended-Spectrum Beta-Lactamase-Producing Escherichia coli From Community-Onset Urinary Tract Infection Cases in Uttarakhand, IndiaCureus2021133e13837

19 

TF Barlam SE Cosgrove LM Abbo C Macdougall AN Schuetz EJ Septimus Implementing an Antibiotic Stewardship Program: Guidelines by the Infectious Diseases Society of America and the Society for Healthcare Epidemiology of AmericaClin Infect Dis Off Publ Infect Dis Soc Am201662105177



jats-html.xsl


This is an Open Access (OA) journal, and articles are distributed under the terms of the Creative Commons Attribution-NonCommercial-ShareAlike 4.0 License, which allows others to remix, tweak, and build upon the work non-commercially, as long as appropriate credit is given and the new creations are licensed under the identical terms.

  • Article highlights
  • Article tables
  • Article images

Article History

Received : 29-07-2024

Accepted : 19-09-2024


View Article

PDF File   Full Text Article


Copyright permission

Get article permission for commercial use

Downlaod

PDF File   XML File   ePub File


Digital Object Identifier (DOI)

Article DOI

https://doi.org/ 10.18231/j.ijmr.2024.048


Article Metrics






Article Access statistics

Viewed: 168

PDF Downloaded: 23