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ORIGINAL ARTICLE
Year : 2021  |  Volume : 65  |  Issue : 3  |  Page : 280-286  

Prevalence of uropathogens and their antimicrobial resistance pattern among adult diabetic patients


1 Senior Resident, Department of General Medicine, Shree Shankaracharya Institute of Medical Sciences, Bhilai, Chhattisgarh, India
2 Professor, Department of General Medicine, Kalinga Institute of Medical Sciences, KIIT University, Bhubaneswar, Odisha, India
3 Scientist-E, Epidemiology Division ICMR-NIIRNCD, Jodhpur, Rajasthan, India
4 Assistant Professor, Department of General Medicine, Kalinga Institute of Medical Sciences, KIIT University, Bhubaneswar, Odisha, India
5 Professor, Department of Microbiology, Kalinga Institute of Medical Sciences, KIIT University, Bhubaneswar, Odisha, India

Date of Submission04-Dec-2020
Date of Decision18-Feb-2021
Date of Acceptance18-Aug-2021
Date of Web Publication22-Sep-2021

Correspondence Address:
Ansuman Panigrahi
Scientist-E, Epidemiology Division, ICMR-NIIRNCD, Jodhpur, Rajasthan
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/ijph.IJPH_1413_20

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   Abstract 


Background: The high prevalence of diabetes, urinary tract infection (UTI) in persons with diabetes, and antibiotic resistance throughout the world including India is a cause of concern for health-care providers. Objectives: The study aimed to assess the prevalence of uropathogens, their resistance pattern, and associated factors of UTI among adults with diabetes. Methods: A cross-sectional study was conducted during the year 2018–2019 among 504 adult diabetic patients attending a tertiary care hospital of Bhubaneswar, Eastern India. Using recommended culture methods, clean-catch midstream urine samples were examined for the presence of pathogenic bacteria and their antimicrobial susceptibility pattern. Results: The prevalence of UTI was 75.4% and the predominant isolates were Escherichia coli (25.6%), Enterococcus spp. (18.7%), and Klebsiella spp. (8.1%). Most of the bacteria isolates were sensitive to nitrofurantoin (80.8%), gentamicin (76.8%), and amikacin (72.1%) whereas resistant to cefpodoxime (77.6%), cefixime (70.8%), and cefadroxil (65.0%). The overall multidrug resistance (MDR) to two or more antimicrobial agents was observed in 87.4% bacterial isolates. The odds of developing UTIs were significantly higher in females with diabetes (adjusted odds ratio [AOR]: 2.04; 95% confidence interval CI: 1.33–3.13), those with Stage I/II hypertension (AOR: 1.77; 95% CI: 1.04–3.008), and those having glycated hemoglobin level >9% (75 mmol) (AOR: 2.15; 95% CI: 1.13–4.10) compared with their counterparts. Conclusion: The prevalence of UTI and MDR to commonly used antibiotics among diabetic patients is alarming, and thus, isolation of uropathogenic bacteria and antimicrobial susceptibility testing is crucial for the treatment of UTI in persons with diabetes.

Keywords: Diabetes mellitus, glycated hemoglobin, hypertension, multidrug resistance, urinary tract infection


How to cite this article:
Kande S, Patro S, Panigrahi A, Khora PK, Pattnaik D. Prevalence of uropathogens and their antimicrobial resistance pattern among adult diabetic patients. Indian J Public Health 2021;65:280-6

How to cite this URL:
Kande S, Patro S, Panigrahi A, Khora PK, Pattnaik D. Prevalence of uropathogens and their antimicrobial resistance pattern among adult diabetic patients. Indian J Public Health [serial online] 2021 [cited 2021 Dec 2];65:280-6. Available from: https://www.ijph.in/text.asp?2021/65/3/280/326384




   Introduction Top


Diabetes mellitus (DM) is a serious public health concern worldwide, affecting about 463 million people, and the number is expected to increase to 578 million by 2030 and 700 million by 2045.[1] It has been estimated that 77 million people have DM in India in 2019 which would rise to 101 million by 2025 and 134.2 million by 2045.[1] DM has been considered as an important risk factor for urinary tract infection (UTI).[2] The reason may be due to higher glucose concentration in urine, which serves as a culture medium for the growth of pathogenic microorganisms,[3],[4] inadequate bladder emptying which necessitates subsequent urological manipulation predisposing UTI,[5] and immunologic impairment.[6] UTI in persons with diabetes may lead to serious complications such as pyelonephritis, multiorgan dysfunction, hypotension, septic shock, sometimes even death.[7]

Various studies have reported that Escherichia coli, Klebsiella spp., Proteus spp., Pseudomonas aeruginosa, Enterococcus spp., Staphylococcus aureus, coagulase-negative staphylococci, Enterobacter spp., and Citrobacter spp. are isolated among DM patients with a varying frequency.[8],[9],[10],[11],[12]

UTI can be successfully managed in persons with diabetes by properly identifying the organisms causing the disease and selecting effective antimicrobial agents against them.[13] The emergence of resistant bacterial strains has been a big challenge to treat and control the spread of infections, especially in low-income countries because of the high prevalence of infection, irrational use of antibiotics, poor infection prevention practices.[11],[14] The high prevalence of DM, UTI in persons with diabetes, and antibiotic resistance throughout the world including India is a cause of concern for health-care providers.[1],[5],[11],[12],[15] Studies on UTI among diabetic patients in India, especially in the eastern region, are scarce.[16],[17] The present study was undertaken to assess the prevalence of uropathogens, their resistance pattern, and associated factors of UTI among adults with diabetes attending a tertiary care hospital of eastern India.


   Materials and Methods Top


Study design, setting, population, and sample size

This descriptive, cross-sectional study was conducted during the year 2018–2019 at a tertiary care hospital of Bhubaneswar, the capital city of Odisha state situated in the eastern part of India. Using universal sampling technique, all adults with diabetes aged 18–70 years who visited the outpatient department of Medicine were considered for the study. Individuals who used antimicrobial for 2 weeks before and during data collection, patients hospitalized for more than 48 h, those with a recent history of catheterization, and pregnant women were excluded from the study. Those having a history of any kind of urosurgery in the past 30 days and known anatomic urologic urinary tract abnormality were also not included in the study. Considering the prevalence of UTI among individuals with diabetes as 45%[5] at a 95% confidence interval (CI) with a margin of error 4.5%, the sample size was calculated as 469. However, 525 eligible adult patients were approached for the study, 21 denied to participate, and finally, 504 were included as study participants.

Data and specimen collection methods

Relevant information including sociodemographic characteristics and laboratory data were collected by the trained investigators using a structured schedule which was developed based on experts' opinions and previous literature. The schedule was validated for its content and language with the help of experts. The schedule in English was first translated into local language (Odia) and then retranslated to English with the help of language experts. Before actual data collection, the pretested schedule was pilot tested on 20 eligible adults with diabetes attending the hospital, and then, the final schedule was prepared after suitable modifications. Each study participant was educated to collect 10–15 ml clean-catch midstream urine sample in a labeled, leak-proof, and sterile container. Within 30 min of collection, all the samples were stored at 4°C and transported to the microbiology laboratory of the hospital within 2 h. A preliminary screening of the uncentrifuged urine was done by making a wet-mount and gram stain to observe the presence of polymorphs and the bacteria.

Culture and identification of bacterial species

Urine samples were directly inoculated on blood agar and MacConkey agar plate or CLED media (media specific instructions were followed for each) using calibrated loops each delivering 0.002 ml of urine. Streaked culture plates were incubated under aerobic conditions at 37°C for 24 h. On the next day, the bacterial growth on the respective media was observed and the total colony count was made. A culture was considered significant for UTI if a single isolated uropathogen was recovered at a concentration of >105 colony-forming units per milliliter of urine. A single colony was picked and suspended in nutrient broth which was incubated at 37°C for further identification. The identification of the bacterial pathogen was done by both manual and automated methods (BactT alert and Vitek2). Identification was done by their colony characteristics on the respective media and pattern of biochemical reactions using the standard procedure.[18]

Antimicrobial susceptibility test

Antimicrobial susceptibility testing was performed using the modified Kirby–Bauer disk diffusion method[19] for manual culture and by VITEK-2 for automated culture. For manual, the bacterial suspension was prepared using nutrient broth by peaking up 3–5 colonies from pure culture and adjusted to 0.5 McFarland standards equal to 108 cells/mL and swab inoculated onto Mueller-Hinton Agar (Oxoid, Ltd., England). Antibiotic impregnated discs were placed onto the surface of the culture medium using an automated disc dispenser. The isolates were tested for ampicillin, amoxicillin-clavulanic acid, ceftriaxone, ciprofloxacin, norfloxacin, cefixime, cefadroxil, cefixime, cefuroxime, cefpodoxime, nitrofurantoin, gentamicin, and sulfamethoxazole + trimethoprim. After 18–24 h of incubation at 37°C, the zone of growth inhibition was measured and interpreted according to the Clinical and Laboratory Standards Institute (CLSI) guideline as susceptible (S), intermediate (I), or resistant (R).[20] The results of culture and antibiotic susceptibility test were validated using the quality control strains of E. coli (ATCC-25922), S. aureus (ATCC 25923), P. aeruginosa (ATCC 27853), and Proteus vulgaris (ATCC 8427).

Statistical analysis

Data were coded, verified, and analyzed usingIBM SPSS Statistics for windows version 21.0 (Armonk, NY:IBM Corp.). Data were expressed as percentage, odds ratio, and 95% CI. Each sociodemographic and clinical characteristic was tested with bivariate logistic regression analysis, and all those found to have a P < 0.1 were included in a multivariate logistic regression model. All P values were two tailed, and P < 0.05 was considered as statistically significant. The authors confirm the availability of, and access to, all original data reported in this study.

Ethical consideration

The study got approval from the Institutional Ethics Committee of the authors' institution (No.KIMS/KIIT/IEC/61/2017, date: September 09, 2017). Written informed consent of all the study participants was sought before their involvement in the study. Based on the laboratory results, the infected participants were appropriately treated.


   Results Top


Characteristics of participants

The mean age of the study participants was 50.5 ± 14.8 years (range: 18–70 years); the majority (62.5%) of them were females and nearly 30% of participants were overweight/obese. Most (61.5%) of the participants had diabetes for ≥5 years and in 17.1% of subjects. Glycated hemoglobin (HbA1c) level was >9% (75 mmol) indicating poor control of diabetes. More than half (57.1%) of the participants had anemia and 83.7% had Stage I/II hypertension. The prevalence of UTI among adults with diabetes was 75.4% (380/504) and 308 (61.1%) were symptomatic. Among the bacteria isolates, E. coli (36.3%), Enterococcus spp. (18.7%), and Klebsiella spp. (8.1%) were the most frequent [Table 1].
Table 1: Characteristics and uropathogenic bacteria isolated from urine specimens of the study participants (n=504)

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Factors associated with urinary tract infection

In bivariate logistic regression analyses, variables such as sex, hypertension, and HbA1c level were statistically associated with UTI at a P < 0.1 and thus included in the multivariate logistic regression model. The multivariate logistic regression analysis revealed that female sex (adjusted odds ratio [AOR]: 2.04; 95% CI: 1.33–3.13), those with Stage I/II hypertension (AOR: 1.77; 95% CI: 1.04–3.008), and those having HbA1c level >9% (AOR: 2.15; 95% CI: 1.13–4.10) were significantly associated with UTI [Table 2].
Table 2: Bivariate and multivariable logistic regression analyses showing association of factors with urinary tract infection among study participants (n=504)

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Antimicrobial susceptibility pattern

Bacteria isolates were sensitive to nitrofurantoin (80.8%), gentamicin (76.8%), and amikacin (72.1%) whereas resistant to cefpodoxime (77.6%), cefixime (70.8%), and cefadroxil (65.0%). E. coli showed higher sensitivity to nitrofurantoin (88%), amikacin (87.4%), and gentamicin (80.3%) while it was resistant to cefpodoxime (78.7%) and cefadroxil (68.9%). Klebsiella spp. showed higher sensitivity to amikacin (73.2%) and gentamicin (70.7%) but resistant to amoxicillin-clavulanic acid (73.2%) and cefpodoxime (68.3%). Enterococcus spp. was highly sensitive to nitrofurantoin (93.6%) and amoxicillin-clavulanic acid (92.6%) but resistant to cotrimoxazole (96.8%), cefpodoxime (84%), and cefixime (81.9%). P. aeruginosa isolates showed higher sensitivity to amikacin (87%) and gentamicin (82.6%) while resistance to nitrofurantoin (87%) and cefixime (78.3%). Staphylococcus spp. showed a higher level of sensitivity to nitrofurantoin (95.7%) followed by amikacin (87.0%), but the highest resistance to cefpodoxime (100%) followed by cefixime (95.7%). Acinetobacter spp. demonstrated the highest sensitivity to levofloxacin (100%) and the highest resistance to nitrofurantoin (100%). Citrobacter spp. showed the highest sensitivity to amikacin (100%), gentamicin (100%), and nitrofurantoin (100%) whereas a considerable degree of resistance against amoxicillin-clavulanic acid (80%) and cefpodoxime (80%). Enterobacter spp. was 100% sensitive to levofloxacin and 100% resistant to amoxicillin-clavulanic acid and cefpodoxime. Proteus mirabilis was 100% sensitive to amikacin, cefixime, ciprofloxacin but highly resistant to amoxicillin-clavulanic acid (66.7%) and cefadroxil (66.7%) [Table 3].
Table 3: In vitro antimicrobial susceptibility pattern of bacteria isolated from urine cultures of study participants (n=380)

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Multidrug resistance

The overall multidrug resistance (MDR), i.e., resistance for ≥ two antimicrobial agents was observed in 87.4% (332/380) bacterial isolates. Thirty (7.9%) of the isolates were resistant to one antibiotic whereas 18 (4.7%) of the isolates were not resistant to any antibiotic agent tested [Table 4].
Table 4: Multiple antimicrobial robial resistance patterns of bacterial isolates from urine culture of study participants (n=380)

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   Discussion Top


The prevalence of UTI observed in the current study is higher compared to result (45%) reported in an earlier study conducted in South India.[5] The prevalence of UTI in our study is also higher compared to previous studies conducted in Ethiopia (16.7–22.6%)[10],[12],[21] and Nepal (50.7%).[22] The difference in prevalence might be explained by geographical variation, sociocultural habits of the community, health awareness, and personal hygiene practices.

In our study, we observed that E. coli was the most frequent bacteria isolate, and this finding is consistent with studies conducted in Ethiopia (31.7%),[10] Tanzania (39%),[23] Iran (43.8%),[8] and India (58%).[5] This might be due to the fact that they are commensals of the bowels, infections are mostly by the fecal contamination and the structure of E. coli, which promotes strong adherence to the uroepithelial cells of individuals with diabetes.[24],[25] The other common isolates in our study were Enterococcus and Klebsiella and this is in agreement with the findings of previous studies.[9],[10],[12],[26]

In this study, the prevalence of MDR was high, which is comparable with the results reported in earlier studies (91.7–95%).[11],[27],[28] The reason for the high prevalence of MDR might be due to patients' poor adherence to antibiotics, their irrational use, and over the counter availability of antibiotics.

We observed in our study that females with diabetes had two times higher odds of having UTI than their male counterparts. This is in accordance with earlier studies.[12],[26],[29] The higher prevalence of UTI among the female population with diabetes may be due to a decrease of normal vaginal flora, less acidic PH of vaginal surface, short urethra, and its proximity to anus.[10],[30],[31]

In the present study, the odds of UTI increase among persons with diabetes having hypertension compared to those without hypertension. Although the exact mechanism behind this association is unknown, it was reported in an earlier study that hypertension was a significant risk factor for UTI among persons with diabetes.[29] Liu et al. also revealed in their study that hypertension can increase urinary bacterial diversity in persons with diabetes.[32]

In this study, individuals with diabetes who had poor diabetic control (HbA1c level >9%) were at a higher risk of developing UTI than those with good diabetic control (HbA1c level ≤9%). Previous studies also reported that UTI was significantly more prevalent in individuals with diabetes having poor glycemic control than in subjects with good glycemic control.[33],[34],[35] The reason might be because higher glucose concentrations in the urine may act as a culture medium for pathogenic bacteria, promote bacterial growth, and its adherence to the urinary tract.[24],[36],[37] Furthermore, genitourinary damage due to diabetes may impair bladder emptying[38] and decrease bladder sensation[39] that can lead to conditions conducive to UTI.

Nevertheless, the study has some limitations. First, the cause-effect relationship between diabetic UTI and other risk factors cannot be established because of the cross-sectional nature of the study. Second, the results of the study may not be representative of the general population with diabetes as it is a single-center hospital-based study. Further validation is anticipated by conducting studies including different hospitals covering a wider geographic region.


   Conclusion Top


The overall prevalence of diabetic UTI was 75.4% and the most common isolates include E. coli, Enterococcus spp., and Klebsiella spp. In view of our study findings, we recommend amikacin, gentamicin, and nitrofurantoin as drug of choice for the treatment of UTI in persons with diabetes based on its demonstrated high sensitivity. MDR to commonly used antibiotics in the study area is alarming, and thus, isolation of uropathogenic bacteria and antimicrobial susceptibility testing is crucial for the treatment of UTI in persons with diabetes. The present study has shown that females with diabetes are at more risk of developing UTI. Similarly, persons with diabetes who are hypertensive and have poor glycemic control have higher odds of getting UTI compared to their counterparts. It underscores the importance of identifying individuals with diabetes who are at high risk of getting UTI and developing strategies to prevent UTI in this vulnerable population.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.



 
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