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 Table of Contents  
Year : 2023  |  Volume : 25  |  Issue : 1  |  Page : 24-28

Changing trend in the clinico- bacteriological profile of diabetic foot infection over a decade: observations from a tertiary care hospital of India

1 MBBS Student, Father Muller Medical College, Mangalore, Karnataka, India
2 Department of Surgery, Father Muller Medical College, Mangalore, Karnataka, India
3 Department of Quality, Father Muller Medical College, Mangalore, Karnataka, India
4 Department of Clinical Microbiology and Infection Control, Father Muller Medical College, Mangalore, Karnataka, India
5 Father Muller Research Centre, Mangalore, Karnataka, India

Date of Submission01-Dec-2022
Date of Decision03-Feb-2023
Date of Acceptance16-Mar-2023
Date of Web Publication1-Jun-2023

Correspondence Address:
Ramakrishna Pai Jakribettu
Department of Microbiology, Malabar Medical College Hospital and Research Centre, Kozhikode, Kerala
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Source of Support: None, Conflict of Interest: None

DOI: 10.4103/jacm.jacm_27_22

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BACKGROUND: Diabetic foot infection (DFI) is a major challenge in podiatric surgery. Initiation of an appropriate antimicrobial drug is the determining factor in the prognosis in DFI.
AIM: This study was undertaken to analyse the changing trends in the clinical profile of patients and the bacterial profile causing DFI for over a decade.
MATERIALS AND METHODS: This was a retrospective observational study conducted at the department of microbiology and surgery of the tertiary teaching hospital. The clinical and bacterial profile of patients with DFI in 2009 and 2019 was collected and analysed for the changing trend.
RESULTS: Amongst the 203 patients (95 in 2009 and 108 in 2019) included in the study, 113 (56%) were male patients. There was a shift in the age group of patients from 51–60 to 61–70 years over a decade. There was a change of most common pathogens from Pseudomonas aeruginosa to Klebsiella species. The resistance rates to third-generation cephalosporins decreased amongst the Gram-negative isolates such as P. aeruginosa and Escherichia coli, but an increase in resistance to carbapenems was observed during the study period. There was reduced incidence of infection with methicillin-resistant Staphylococcus aureus during the study period.
CONCLUSION: There was a change in the demographic and bacteriological flora in the DFI patients over a decade. The antimicrobial resistance rate varied for various antimicrobial agents over a decade for a particular pathogen. Regular surveillance of the change in resistance pattern amongst the pathogens is essential for the initiation of appropriate empirical therapy to reduce the morbidity in DFI.

Keywords: Anti-microbial resistance, decade, diabetic foot, Klebsiella species, trend

How to cite this article:
Pais ML, D'Souza RC, Surlu VR, Boloor R, Baliga MS, Jakribettu RP. Changing trend in the clinico- bacteriological profile of diabetic foot infection over a decade: observations from a tertiary care hospital of India. J Acad Clin Microbiol 2023;25:24-8

How to cite this URL:
Pais ML, D'Souza RC, Surlu VR, Boloor R, Baliga MS, Jakribettu RP. Changing trend in the clinico- bacteriological profile of diabetic foot infection over a decade: observations from a tertiary care hospital of India. J Acad Clin Microbiol [serial online] 2023 [cited 2023 Nov 30];25:24-8. Available from: https://www.jacmjournal.org/text.asp?2023/25/1/24/378067

  Introduction Top

Anti-microbial resistance (AMR) is a global threat as the pathogens are evolving at a higher rate than the rate of discovery of newer antimicrobial agents (AMA). Amongst the vulnerable patients, infection with multidrug-resistant (MDR) pathogens results in prolonged duration of illness with increased morbidity and mortality.[1] The emergence of the AMR in community is not only attributed to overuse/misuse and inappropriate use of AMA in the healthcare sector but also to overuse of these AMA as growth factors in animal husbandry.[2] This phenomenon has a very high impact on the healthcare sector and society, at large.

Active surveillance of AMR at the regional, national, community as well as hospital level can help us in early detection, treatment and control of spread of MDR pathogens efficiently.[2] Amongst the vulnerable patients, who are predisposed to common bacterial infections, are the patients with uncontrolled diabetes mellitus. India, the diabetic capital of the world, is estimated to have nearly 69.9 million and 80 million diabetic patients by the year 2025 and 2030, respectively.[3]

Clinically, amongst the various complications in diabetes mellitus, foot infection is the most common and associated with high morbidity.[4] Diabetic foot infection (DFI) is associated with hyperglycaemia-induced metabolic abnormalities and atherosclerosis leading to neuropathy and vascular disease.[5] The reduced blood flow to the site of infection causes reduced delivery of AMA and thus delays in the eradication of pathogens and wound healing. Moreover, inappropriate initial antimicrobial therapy can cause delay in treatment of infection.[6] Currently, it is known that the DFI is caused by various pathogens that may vary from different geographical area, which keeps on altering depending on the usage of AMA. A regular surveillance of the change in bacterial flora causing infection and their drug resistance pattern needs to be done to initiate appropriate antibacterial therapy. Hence, this study was undertaken with an objective to analyse the change in the bacterial pathogens and their AMR pattern causing DFI for over a decade in the patients admitted in the tertiary care teaching hospital.

  Materials and Methods Top

This was a retrospective record-based study conducted in the department of microbiology and surgery of a tertiary care teaching hospital after obtaining clearance from the institutional ethical committee (FMIEC/CCM/96/2021). All patients who were diagnosed with DFIs in 2009 and 2019 were included in the study. The demographic details, history of diabetes mellitus and co-morbidities were noted. The grading of the diabetic foot was done as per the Wagner's classification.[7] The details of the bacterial growth from the wound biopsy/swab were noted in the microbiology laboratory. The bacterial isolates from the samples with numerous pus cells and no epithelial cells in the Gram stain were considered pathogens and were included in the study. The pathogens isolated from the samples with few or scanty pus cells with the presence of epithelial cells were considered colonisers and were excluded from the study. The antibacterial susceptibility test was conducted by Kirby–Bauer's disc diffusion test as per the Clinical and Laboratory Standards Institute (CLSI) guidelines of the respective year (CLSI 2009, 2019).[8],[9] The details were entered into the Microsoft Excel software and analysed by the frequency and percentage.

  Results Top

A total of 203 were admitted to the hospital with DFIs, 95 in 2009 and 108 in 2019. The male patients were three times than females in both years [Table 1]. There was an increase in around 11% of occurrence in female patients over a decade. Most of the patients belonged to the age group of 51–60 years in 2009 (36%) and 61–70 years in 2019 (39%). In 2009, nearly 40% of DFI patients reported having diabetes for 6–10 years, whereas in 2019, patients had diabetes for more than 10 years (40%). There was a shift by 10 years in the age group of patients with DFI from 2009 to 2019.
Table 1: Demographic and clinical details of the diabetic foot patients studied in 2009 and 2019

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Amongst the patients included in the study in 2009 and 2019, no co-morbidities were noted in around 55% and 41% of patients, respectively. The patients with two and more co-morbidities were around 13% and 26% in 2009 and 2019, respectively [Table 1]. The co-morbidities such as hypertension, ischaemic heart disease and chronic kidney disease were reported higher amongst DFI in 2019 compared to 2009 [Table 1]. Similarly, patients with both insulin and oral hypoglycaemic drugs were nearly 15% (2009) and 37% (2019), respectively [Table 1]. The complications of diabetes mellitus such as retinopathy, nephropathy and neuropathy were reported in both groups of patients. The most of DFI patients were of Wagner Classification of 1 and 3 in 2009 and 2 and 4 in 2019 [Table 1]. The samples from DFI patients were received as exudate/pus, wound swab, wound biopsy and distribution of the same is shown in [Table 1]. In 2009, five patients had polymicrobial infection compared to 23 in 2019 [Table 1].

During the study period, 103 and 189 bacteria were grown in culture from the patients of DFI in 2009 and 2019, respectively amongst which 11 and 23 were excluded as they were considered colonisers, as the samples showed more epithelial cells and less pus cells. Hence, 92 and 166 bacterial isolates were considered pathogens and were included in the study for the years 2009 and 2019, respectively [Table 2]. Amongst the pathogens isolated, gram-negative bacteria outnumbered in both groups of patients. Pseudomonas aeruginosa (17%) and Klebsiella species (11%) were most common in 2009, but in 2019, Klebsiella sp. (19%) was the highest isolated followed by Pseudomonas sp. (16%). Amongst the Gram-positive pathogens, Staphylococcus aureus and Enterococcus sp. were common in 2009. In 2019, the isolation of β-haemolytic Streptococcus was more compared to 2009 [Table 2].
Table 2: Change in distribution of various pathogens isolated amongst the diabetic foot infection patients in 2009 and 2019

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Amongst the most common Gram-negative pathogen, P. aeruginosa, there was an increase in resistance rate to amikacin, ciprofloxacin and meropenem. In Klebsiella sp., there was an increase in the resistance rate to third-generation cephalosporins (3GC), amikacin, ciprofloxacin, piperacillin/tazobactam and meropenem [Table 3]. Amongst the Gram-positive pathogens, S. aureus outnumbered. There was a steady decline in the isolation rate of methicillin-resistant S. aureus (MRSA) observed from 41% to 25% as per the appropriate CLSI guidelines of respective years. There was a steady decline in resistance to co-trimoxazole, gentamicin and ciprofloxacin, but increased resistance was observed for erythromycin and clindamycin [Table 3].
Table 3: Change in resistance pattern to various antimicrobial agents in most common pathogens isolated amongst the diabetic foot infection patients in 2009 and 2019

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  Discussion Top

This is the first study that compares the demographic, clinical and bacteriological profile of patients with DFIs over a decade in a tertiary care centre in India. It is most important to identify the pathogens amongst the colonisers in bacterial culture, as mere isolation of bacteria from diabetic wounds may not be a representative flora of infections. Therefore, we have correlated with the isolates with nature of the sample received depending on the presence of polymorphonuclear cells and epithelial cells in Gram-stained smear of the sample. In our study, male patients were three times higher than female patients, as seen in other study populations where the male had two to three times higher incidence of DFI than female patients.[10],[11] The female patients with DFI doubled in a decade from 12% in 2009 to 24% in 2019. Many studies had patients in their 6th decade of life presenting with DFI, similar to our observation.[12] The prevalence of DFI varies depending on the population studied and the number of years of diabetes.[11],[13] Most of our patients presented with DFI were diagnosed with diabetes for >10 years. The comorbidities, such as hypertension, ischaemic heart disease and chronic kidney disease associated with diabetes mellitus,[14] are increasingly reported with patients with DFI. Over a decade, we have observed the change in the Wagner grading of diabetic foot, especially in Grade 2 and 4. With increase in the grade of Wagner classification, the incidence of infection is higher.[15]

Over the decade, the Gram-negative bacilli have been the predominant pathogens causing DFI amongst our patients. There was even reduction in the Gram-positive cocci over 10% during the study period. The Gram-negative bacilli have been a predominant pathogen in most of the studies from developing countries.[11] In 2009, P. aeruginosa was predominant followed by Escherichia coli, Klebsiella sp., but the flora changed to Klebsiella sp., P. aeruginosa and E. coli in decreasing incidence rate in 2019. This emphasis on the need of continuous surveillance for the change in the flora causing DFI as it is crucial for starting appropriate empirical antimicrobial therapy.

Studies in different populations revealed P. aeruginosa, Klebsiella and E. coli as common pathogens with varying percentages of incidence.[11],[12] Amongst the Gram-positive, S. aureus and Enterococcus sp. were prominent in 2009, but in 2019, βhaemolytic Streptococcus was the second most common isolate following S. aureus.[16] Gram-positive cocci as the predominant pathogen were reported in a few studies, mainly from developed countries.[17]

Amongst the individual pathogen, it was observed to have changing trend in resistance. Overall, there was an increase in resistance for all AMA amongst the Gram-negative pathogen, except P. aeruginosa to 3GC, βL-βLI; E. coli to 3GC, Amikacin. On the contrary, there was a decreasing trend of resistance in Gram-positive pathogens. The prevalence of MRSA amongst the patients have reduced, this is similar to other studies in Asian population.[18] These changes in the resistance pattern are of concern at the community level.[19]

This study has revealed the change in the microbial flora causing DFI at our community level over a decade. There is a trend of emerging resistance to the high-end AMA such as 3GC, βL-βLI carbapenem, which is alarming. Hence, these high-end AMA drug needs to be used cautiously in the patients to prevent a further rise in resistance pattern. The changing trend of resistance patterns to various AMA emphasises the need for effective antimicrobial stewardship programmes at the national and global levels in the community.[2] As this was a retrospective study, the dynamics of antimicrobial administration and its effect on the microbial flora were not studied. During the study period, anaerobic bacterial culture was not done; hence in this study, we are not able to determine the anaerobic flora causing DFI. Being a single-centric study, validation of the results needs to be done by a multi-centric study with a larger population, so as the antibiotic policy can be formulated for a population of particular geographical area.

  Conclusion Top

A change in the trend of DFI with an increased incidence amongst females, mainly in the 7th decade of life was noted in our study. The prevalence of DFI was seen higher amongst the patients with >10 years of treatment with oral hypoglycaemic agents and insulin. Patients with hypertension and ischaemic heart disease had a higher incidence of DFI. Predominantly, gram-negative pathogens have been causing infection for over a decade, but the genus causing infection is dynamic. There is also increasing resistance amongst the first and second line of antimicrobials and there is an emergence of resistance to higher-end AMA such as βL-βLI and carbapenems over a decade. These data will help us to formulate an appropriate policy for the effective implementation of the antimicrobial stewardship programme in DFI patients.

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Conflicts of interest

There are no conflicts of interest.

  References Top

World Health Organization. Antimicrobial Resistance: Global Report on Surveillance. Geneva: World Health Organization; 2014.  Back to cited text no. 1
World Health Organization. Monitoring and Evaluation of the Global Action Plan on Antimicrobial Resistance: Framework and Recommended Indicators. Geneva: World Health Organization; 2019.  Back to cited text no. 2
Kaveeshwar SA, Cornwall J. The current state of diabetes mellitus in India. Australas Med J 2014;7:45-8.  Back to cited text no. 3
Dietrich I, Braga GA, de Melo FG, da Costa Silva Silva AC. The diabetic foot as a proxy for cardiovascular events and mortality review. Curr Atheroscler Rep 2017;19:44.  Back to cited text no. 4
Thiruvoipati T, Kielhorn CE, Armstrong EJ. Peripheral artery disease in patients with diabetes: Epidemiology, mechanisms, and outcomes. World J Diabetes 2015;6:961-9.  Back to cited text no. 5
Lipsky BA. Diabetic foot infections: Current treatment and delaying the 'post-antibiotic era'. Diabetes Metab Res Rev 2016;32 Suppl 1:246-53.  Back to cited text no. 6
Frykberg RG. Diabetic foot ulcers: Pathogenesis and management. Am Fam Physician 2002;66:1655-62.  Back to cited text no. 7
Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. 19th ed. CLSI supplement M100. Clinical and Laboratory Standards Institute, USA, 2009.  Back to cited text no. 8
Clinical and Laboratory Standards Institute (CLSI). Performance Standards for Antimicrobial Susceptibility Testing. CLSI Supplement M100. 29th ed. USA: Clinical and Laboratory Standards Institute; 2019.  Back to cited text no. 9
Saseedharan S, Sahu M, Chaddha R, Pathrose E, Bal A, Bhalekar P, et al. Epidemiology of diabetic foot infections in a reference tertiary hospital in India. Braz J Microbiol 2018;49:401-6.  Back to cited text no. 10
Chai W, Wang Y, Zheng H, Yue S, Liu Y, Wu Y, et al. The profile of microbiological pathogens in diabetic foot ulcers. Front Med (Lausanne) 2021;8:656467.  Back to cited text no. 11
Seth A, Attri AK, Kataria H, Kochhar S, Seth SA, Gautam N. Clinical profile and outcome in patients of diabetic foot infection. Int J Appl Basic Med Res 2019;9:14-9.  Back to cited text no. 12
Ahmadishooli A, Davoodian P, Shoja S, Ahmadishooli B, Dadvand H, Hamadiyan H, et al. Frequency and antimicrobial susceptibility patterns of diabetic foot infection of patients from Bandar Abbas district, Southern Iran. J Pathog 2020;2020:1057167.  Back to cited text no. 13
Honda Y, Wakabayashi K, Sato C, Ikeda N, Sato K, Suzuki T, et al. Chronic kidney disease is a key predictive factor for potential myocardial ischaemia and poor prognosis in asymptomatic patients with diabetes mellitus. Sci Rep 2022;12:10268.  Back to cited text no. 14
Shah P, Inturi R, Anne D, Jadhav D, Viswambharan V, Khadilkar R, et al. Wagner's classification as a tool for treating diabetic foot ulcers: Our observations at a suburban teaching hospital. Cureus 2022;14:e21501.  Back to cited text no. 15
Rampal SR, Devaraj NK, Yoganathan PR, Mahusin MA, Teh SW, Kumar SS. Distribution and prevalence of microorganisms causing diabetic foot infection in hospital Serdang and hospital Ampang for the year 2010 to 2014. Biocatal Agric Biotechnol 2019;17:256-60.  Back to cited text no. 16
Lipsky BA, Aragón-Sánchez J, Diggle M, Embil J, Kono S, Lavery L, et al. IWGDF guidance on the diagnosis and management of foot infections in persons with diabetes. Diabetes Metab Res Rev 2016;32 Suppl 1:45-74.  Back to cited text no. 17
Lee JS, Son ST, Han SK. Risk factors of methicillin-resistant Staphylococcus aureus and Pseudomonas infection in diabetic foot ulcers in Korea. J Wound Manage Res 2017;13:29-34.  Back to cited text no. 18
Kwon KT, Armstrong DG. Microbiology and antimicrobial therapy for diabetic foot infections. Infect Chemother 2018;50:11-20.  Back to cited text no. 19


  [Table 1], [Table 2], [Table 3]


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