Microbiological profile of diabetic foot ulcers in Kuwait

Asma Alhubail 1, May Sewify 1, Grace Messenger 1, Richard Masoetsa 1, Imtiaz Hussain 1, Shinu Nair 1, Ali Tiss 2

Affiliations

30 December 2020

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doi: 10.1371/journal.pone.0244306

Abstract

Introduction: Diabetic foot ulcers (DFU) and infection (DFI) are a major diabetes-related problem around the world due to the high prevalence of diabetes in the population. The aim of our study was to determine the microbiological profile of infected ulcers in patients attending Dasman Diabetes Institute (DDI) clinics in Kuwait and to analyze the distribution of microbial isolates according to wound grade, sex, age and diabetes control.

Methods: We collected and analyzed clinical data and samples from 513 diabetic patients with foot ulcers referred to our podiatry clinic at DDI from Jan 2011 till Dec 2017.

Results: We show a higher prevalence of DFU in men than in women, and a greater percentage of DFU occurred in men at an earlier age (p<0.05). Only about half of the DFU were clinically infected (49.3%) but 92% of DFU showed bacterial growth in the microbiological lab analysis. In addition, we isolated more monomicrobial (57.3%) than polymicrobial (34.8%) DFI and representing an average of 1.30 pathogens per patient. The presence of Gram-positive and Gram-negative strains was comparable between men and women regardless their age or glucose levels. Interestingly, more Gram-positive strains are present in ulcers without ischemia while more Gram-negative strains are present in ulcers with ischemia (p<0.05). While Staphylococcus aureus was common in infected ulcers without ischemia, Pseudomonas aeruginosa was predominant in ulcers with infection and ischemia, regardless of ulcer depth. Finally, a higher percentage of women has controlled HbA1c levels (19.41% versus 11.95% in men) and more women in this group displayed non-infected wounds (60.6% and 43.90% for women and men, respectively).

Conclusion: Our results provide an updated picture of the DFI patterns and antibiotics resistance in patients attending Dasman Diabetes Institute (DDI) clinics in Kuwait which might help in adopting the appropriate treatment of infected foot and improving clinical outcomes.

Conflict of interest statement

The authors have declared that no competing interests exist.

Figures

Fig 1. Wound grading distribution among the DFU study population. Patient DFU were classified according to the University of Texas Wound Grading Classification System which grades them depending on the presence or absence of infection and ischemia, as detailed in Material and Methods section.

Fig 1. Wound grading distribution among the DFU study population. Patient DFU were classified according to the University of Texas Wound Grading Classification System which grades them depending on the presence or absence of infection and ischemia, as detailed in Material and Methods section.

Fig 2. Main species distribution among the study population with clinically infected wounds. The species distribution was calculated as percentage of the total number of isolates within the same wound grade.

Fig 2. Main species distribution among the study population with clinically infected wounds. The species distribution was calculated as percentage of the total number of isolates within the same wound grade.

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References

  1.  
    1. Ramsey SD, Newton K, Blough D, McCulloch DK, Sandhu N, Reiber GE, et al.: Incidence, outcomes, and cost of foot ulcers in patients with diabetes. Diabetes Care 1999, 22:382–387. 10.2337/diacare.22.3.382 - DOI - PubMed
  2.  
    1. Reiber GE, Smith DG, Carter J, Fotieo G, Deery HG 2nd, Sangeorzan JA, et al.: A comparison of diabetic foot ulcer patients managed in VHA and non-VHA settings. J Rehabil Res Dev 2001, 38:309–317. - PubMed
  3.  
    1. Lavery LA, Armstrong DG, Wunderlich RP, Tredwell J, Boulton AJ: Diabetic foot syndrome: evaluating the prevalence and incidence of foot pathology in Mexican Americans and non-Hispanic whites from a diabetes disease management cohort. Diabetes Care 2003, 26:1435–1438. 10.2337/diacare.26.5.1435 - DOI - PubMed
  4.  
    1. Epicast: EpiCast Report: Diabetic Foot Ulcers—Epidemiology Forecast to 2025. pp. 1–59; 2017:1–59.
  5.  
    1. IDF: IDF Diabetes Atlas. vol. 9th edition pp. 1–176: International Diabetes Federation; 2019:1–176.
  6.  
    1. Messenger G, Masoetsa R, Hussain I, Devarajan S, Jahromi M: Diabetic foot ulcer outcomes from a podiatry led tertiary service in Kuwait. Diabet Foot Ankle 2018, 9:1471927 10.1080/2000625X.2018.1471927 - DOI - PMC - PubMed
  7.  
    1. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, et al.: High prevalence of ischaemia, infection and serious comorbidity in patients with diabetic foot disease in Europe. Baseline results from the Eurodiale study. Diabetologia 2007, 50:18–25. 10.1007/s00125-006-0491-1 - DOI - PubMed
  8.  
    1. Jia L, Parker CN, Parker TJ, Kinnear EM, Derhy PH, Alvarado AM, et al.: Incidence and risk factors for developing infection in patients presenting with uninfected diabetic foot ulcers. PLoS One 2017, 12:e0177916 10.1371/journal.pone.0177916 - DOI - PMC - PubMed
  9.  
    1. Lipsky BA, Berendt AR, Cornia PB, Pile JC, Peters EJ, Armstrong DG, et al.: 2012 Infectious Diseases Society of America clinical practice guideline for the diagnosis and treatment of diabetic foot infections. Clin Infect Dis 2012, 54:e132–173. 10.1093/cid/cis346 - DOI - PubMed
  10.  
    1. Hicks CW, Selvarajah S, Mathioudakis N, Sherman RE, Hines KF, Black JH 3rd, et al.: Burden of Infected Diabetic Foot Ulcers on Hospital Admissions and Costs. Ann Vasc Surg 2016, 33:149–158. 10.1016/j.avsg.2015.11.025 - DOI - PMC - PubMed
  11.  
    1. Sugandhi P, Prasanth DA: Bacteriological Profile of Diabetic Foot. International Journal of Innovative Research in Science 2014, 3:14688–14692.
  12.  
    1. Fair RJ, Tor Y: Antibiotics and bacterial resistance in the 21st century. Perspect Medicin Chem 2014, 6:25–64. 10.4137/PMC.S14459 - DOI - PMC - PubMed
  13.  
    1. Abdulrazak A, Bitar ZI, Al-Shamali AA, Mobasher LA: Bacteriological study of diabetic foot infections. J Diabetes Complications 2005, 19:138–141. 10.1016/j.jdiacomp.2004.06.001 - DOI - PubMed
  14.  
    1. Citron DM, Goldstein EJ, Merriam CV, Lipsky BA, Abramson MA: Bacteriology of moderate-to-severe diabetic foot infections and in vitro activity of antimicrobial agents. J Clin Microbiol 2007, 45:2819–2828. 10.1128/JCM.00551-07 - DOI - PMC - PubMed
  15.  
    1. Al Benwan K, Al Mulla A, Rotimi VO: A study of the microbiology of diabetic foot infections in a teaching hospital in Kuwait. J Infect Public Health 2012, 5:1–8. 10.1016/j.jiph.2011.07.004 - DOI - PubMed
  16.  
    1. Lipsky BA, Itani K, Norden C, Linezolid Diabetic Foot Infections Study G: Treating foot infections in diabetic patients: a randomized, multicenter, open-label trial of linezolid versus ampicillin-sulbactam/amoxicillin-clavulanate. Clin Infect Dis 2004, 38:17–24. 10.1086/380449 - DOI - PubMed
  17.  
    1. Viswanathan V, Pendsey S, Radhakrishnan C, Rege TD, Ahdal J, Jain R: Methicillin-Resistant Staphylococcus aureus in Diabetic Foot Infection in India: A Growing Menace. Int J Low Extrem Wounds 2019:1534734619853668 10.1177/1534734619853668 - DOI - PubMed
  18.  
    1. Neves JM, Duarte B, Pinto M, Formiga A, Neves J: Diabetic Foot Infection: Causative Pathogens and Empiric Antibiotherapy Considerations-The Experience of a Tertiary Center. Int J Low Extrem Wounds 2019:1534734619839815 10.1177/1534734619839815 - DOI - PubMed
  19.  
    1. Shankar EM, Mohan V, Premalatha G, Srinivasan RS, Usha AR: Bacterial etiology of diabetic foot infections in South India. Eur J Intern Med 2005, 16:567–570. 10.1016/j.ejim.2005.06.016 - DOI - PubMed
  20.  
    1. Ertugrul BM, Lipsky BA, Ture M, Sakarya S: Risk Factors for Infection with Pseudomonas aeruginosa in Diabetic Foot Infections. J Am Podiatr Med Assoc 2017, 107:483–489. 10.7547/15-167 - DOI - PubMed
  21.  
    1. Dunyach-Remy C, Ngba Essebe C, Sotto A, Lavigne JP: Staphylococcus aureus Toxins and Diabetic Foot Ulcers: Role in Pathogenesis and Interest in Diagnosis. Toxins (Basel) 2016, 8 10.3390/toxins8070209 - DOI - PMC - PubMed
  22.  
    1. Pereira SG, Moura J, Carvalho E, Empadinhas N: Microbiota of Chronic Diabetic Wounds: Ecology, Impact, and Potential for Innovative Treatment Strategies. Front Microbiol 2017, 8:1791 10.3389/fmicb.2017.01791 - DOI - PMC - PubMed
  23.  
    1. Lipsky BA: Diabetic foot infections: Current treatment and delaying the ‘post-antibiotic era'. Diabetes Metab Res Rev 2016, 32 Suppl 1:246–253. 10.1002/dmrr.2739 - DOI - PubMed
  24.  
    1. Armstrong DG, Lavery LA, Harkless LB: Validation of a diabetic wound classification system. The contribution of depth, infection, and ischemia to risk of amputation. Diabetes Care 1998, 21:855–859. 10.2337/diacare.21.5.855 - DOI - PubMed
  25.  
    1. Levine NS, Lindberg RB, Mason AD Jr., Pruitt BA Jr.: The quantitative swab culture and smear: A quick, simple method for determining the number of viable aerobic bacteria on open wounds. J Trauma 1976, 16:89–94. - PubMed
  26.  
    1. Bauer AW, Kirby WM, Sherris JC, Turck M: Antibiotic susceptibility testing by a standardized single disk method. Am J Clin Pathol 1966, 45:493–496. - PubMed
  27.  
    1. Shakil S, Khan AU: Infected foot ulcers in male and female diabetic patients: a clinico-bioinformative study. Ann Clin Microbiol Antimicrob 2010, 9:2 10.1186/1476-0711-9-2 - DOI - PMC - PubMed
  28.  
    1. Patil S, Mane R: Bacterial and clinical profile of diabetic foot ulcer using optimal culture techniques. International Journal of Research in Medical Sciences 2017, 5:496–502.
  29.  
    1. Mendes JJ, Marques-Costa A, Vilela C, Neves J, Candeias N, Cavaco-Silva P, et al.: Clinical and bacteriological survey of diabetic foot infections in Lisbon. Diabetes Res Clin Pract 2012, 95:153–161. 10.1016/j.diabres.2011.10.001 - DOI - PubMed
  30.  
    1. 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, 49:401–406. 10.1016/j.bjm.2017.09.003 - DOI - PMC - PubMed
  31.  
    1. Tascini C, Piaggesi A, Tagliaferri E, Iacopi E, Fondelli S, Tedeschi A, et al.: Microbiology at first visit of moderate-to-severe diabetic foot infection with antimicrobial activity and a survey of quinolone monotherapy. Diabetes Res Clin Pract 2011, 94:133–139. 10.1016/j.diabres.2011.07.017 - DOI - PubMed
  32.  
    1. Tiwari S, Pratyush DD, Dwivedi A, Gupta SK, Rai M, Singh SK: Microbiological and clinical characteristics of diabetic foot infections in northern India. J Infect Dev Ctries 2012, 6:329–332. 10.3855/jidc.1827 - DOI - PubMed
  33.  
    1. Rahim F, Ullah F, Ishfaq M, Afridi AK, Rahman SU, Rahman H: Frequency Of Common Bacteria And Their Antibiotic Sensitivity Pattern In Diabetics Presenting With Foot Ulcer. J Ayub Med Coll Abbottabad 2016, 28:528–533. - PubMed
  34.  
    1. Prompers L, Huijberts M, Apelqvist J, Jude E, Piaggesi A, Bakker K, et al.: Delivery of care to diabetic patients with foot ulcers in daily practice: results of the Eurodiale Study, a prospective cohort study. Diabet Med 2008, 25:700–707. 10.1111/j.1464-5491.2008.02445.x - DOI - PubMed
  35.  
    1. Xie X, Bao Y, Ni L, Liu D, Niu S, Lin H, et al.: Bacterial Profile and Antibiotic Resistance in Patients with Diabetic Foot Ulcer in Guangzhou, Southern China: Focus on the Differences among Different Wagner’s Grades, IDSA/IWGDF Grades, and Ulcer Types. Int J Endocrinol 2017, 2017:8694903 10.1155/2017/8694903 - DOI - PMC - PubMed
  36.  
    1. Huang Y, Cao Y, Zou M, Luo X, Jiang Y, Xue Y, et al.: A Comparison of Tissue versus Swab Culturing of Infected Diabetic Foot Wounds. Int J Endocrinol 2016, 2016:8198714 10.1155/2016/8198714 - DOI - PMC - PubMed
  37.  
    1. Gardiner M, Vicaretti M, Sparks J, Bansal S, Bush S, Liu M, et al.: A longitudinal study of the diabetic skin and wound microbiome. PeerJ 2017, 5:e3543 10.7717/peerj.3543 - DOI - PMC - PubMed
  38.  
    1. Chambers HF, Deleo FR: Waves of resistance: Staphylococcus aureus in the antibiotic era. Nat Rev Microbiol 2009, 7:629–641. 10.1038/nrmicro2200 - DOI - PMC - PubMed
  39.  
    1. EARSS: European Antimicrobial Resistance Surveillance System. The Netherlands; 2007.
  40.  
    1. Kinross P, Petersen A, Skov R, Van Hauwermeiren E, Pantosti A, Laurent F, et al.: Livestock-associated meticillin-resistant Staphylococcus aureus (MRSA) among human MRSA isolates, European Union/European Economic Area countries, 2013. Euro Surveill 2017, 22 10.2807/1560-7917.ES.2017.22.44.16-00696 - DOI - PMC - PubMed
  41.  
    1. Tsiodras S, Gold HS, Sakoulas G, Eliopoulos GM, Wennersten C, Venkataraman L, et al.: Linezolid resistance in a clinical isolate of Staphylococcus aureus. Lancet 2001, 358:207–208. 10.1016/S0140-6736(01)05410-1 - DOI - PubMed
  42.  
    1. Wilson P, Andrews JA, Charlesworth R, Walesby R, Singer M, Farrell DJ, et al.: Linezolid resistance in clinical isolates of Staphylococcus aureus. J Antimicrob Chemother 2003, 51:186–188. 10.1093/jac/dkg104 - DOI - PubMed
  43.  
    1. Crouzet J, Lavigne JP, Richard JL, Sotto A, Nimes University Hospital Working Group on the Diabetic F: Diabetic foot infection: a critical review of recent randomized clinical trials on antibiotic therapy. Int J Infect Dis 2011, 15:e601–610. 10.1016/j.ijid.2011.05.003 - DOI - PubMed
  44.  
    1. Shanthi M, Sekar U, Kamalanathan A, Sekar B: Detection of New Delhi metallo beta lactamase-1 (NDM-1) carbapenemase in Pseudomonas aeruginosa in a single centre in southern India. Indian J Med Res 2014, 140:546–550. - PMC - PubMed
  45.  
    1. Sotto A, Richard JL, Combescure C, Jourdan N, Schuldiner S, Bouziges N, et al.: Beneficial effects of implementing guidelines on microbiology and costs of infected diabetic foot ulcers. Diabetologia 2010, 53:2249–2255. 10.1007/s00125-010-1828-3 - DOI - PubMed

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