Abstract

Background: Complications of infected wounds in patients with diabetic foot ulcer (DFU) are one of the greatest challenges in modern medicine. Analysis of the microbiological profile of infected ulcers may significantly improve treatment results. The aim of the study was to determine the profile of pathogens isolated in patients with DFU and to compare the results of other centers. Materials and Methods: A retrospective study was carried out on 137 patients with DFU hospitalized at the Department of Diabetology and Internal Diseases, Medical University of Warsaw in 2011-2014. The analysis included the results of 200 microbiological cultures tested for fungi, aerobic and anaerobic bacteria. Statistical analysis was used to test differences in HbA1c values in relation to the strain of the most commonly cultured bacteria and the relationship between glycemic control and most frequently isolated pathogens. Results: Seventy-nine bacterial species were isolated in 183 positive cultures. Gram-negative bacteria predominated with the highest percentage of representatives of Enterobacterales. The most often isolated bacteria were Serratia marcescens, Pseudomonas aeruginosa, Proteus mirabilis and methicillin-susceptible Staphylococcus aureus. The Kruskal-Wallis test revealed that HbA1c concentrations were different in groups infected with different strains of bacteria (p = 0.0087). Isolation of Escherichia coli and Morganella morganii was more often associated with poor control of diabetes. Conclusions: The study revealed statistically significant differences in the frequency of microorganisms isolated from the wounds of patients with DFU. The discrepancies in the results of other studies published in this field indicate the need for standardization of the research design.

References

• 1. Adeolu M., Alnajar S., Naushad S., Gupta R.S.: Genome-basedphylogeny and taxonomy of the ‘Enterobacteriales’: proposal for Enterobacteralesord. nov. divided into the families Enterobacteriaceae,Erwiniaceae fam. nov., Pectobacteriaceae fam. nov., Yersiniaceae fam.nov., Hafniaceae fam. nov., Morganellaceae fam. nov., and Budviciaceaefam. nov. Int. J. Syst. Evol. Microbiol., 2016; 66: 5575–5599
  Google Scholar
• 2. Al Benwan K., Al Mulla A., Rotimi V.O.: A study of the microbiologyof diabetic foot infections in teaching hospital in Kuweit. J.Infec. Public Health, 2012; 5: 1–8
  Google Scholar
• 3. Bendy R.H.Jr., Nuccio P.A., Wolfe E., Collins B., Tamburro C.,Glass W., Martin C.M.: Relationship of quantitative wound bacterialcounts to healing of decubiti: Effect of topical gentamicin.Antimicrob. Agents Chemother., 1964; 10: 147–155
  Google Scholar
• 4. Bowler P.G., Duerden B.I., Armstrong D.G.: Wound microbiologyand associated approaches to wound management. Clin. Microbiol.Rev., 2001; 14: 244–269
  Google Scholar
• 5. Citron D.M., Goldstein E.J.C., Merriam C.V., Lipsky B.A., AbramsonM.A.: Bacteriology of moderate-to-severe diabetic foot infectionsand in vitro activity of antimicrobial agents. J. Clin. Microbiol.,2007; 45: 2819–2828
  Google Scholar
• 6. Crouzet J., Lavigne J.P., Richard J.L., Sotto A., Nîmes UniversityHospital Working Group on the Diabetic Foot (GP30): Diabetic footinfection: A critical review of recent randomized clinical trials onantibiotic therapy. Int. J. Infect. Dis., 2011; 15: e601–e610
  Google Scholar
• 7. Dowd S.E., Wolcott R.D., Sun Y., McKeehan T., Smith E., RhoadsD.: Polymicrobial nature of chronic diabetic foot ulcer biofilm infectionsdetermined using bacterial tag encoded FLX ampliconpyrosequencing (bTEFAP). PLoS One, 2008; 3: e3326
  Google Scholar
• 8. Gadepalli R., Dhawan B., Sreenivas V., Kapil A., Ammini A.C.,Chaudhry R.: A clinico-microbiological study of diabetic footulcers in an Indian tertiary care hospital. Diabetes Care, 2006;29: 1727–1732
  Google Scholar
• 9. Gardner S.E., Hillis S.L., Heilmann K., Segre J.A., Grice E.A.:The neuropathic diabetic foot ulcer microbiome is associatedwith clinical factors. Diabetes, 2013; 62: 923–930
  Google Scholar
• 10. Geerlings S.E., Hoepelman A.I.: Immune dysfunction in patientswith diabetes mellitus (DM). FEMS Immunol. Med. Microbiol.,1999; 26: 259–265
  Google Scholar
• 11. Hadadi A., Omdeh Ghiasi H., Hajiabdolbaghi M., ZandekarimiM., Hamidian R.: Diabetic foot: Infections and outcomes in Iranianadmitted patients. Jundishapur J. Microbiol., 2014; 7: e11680
  Google Scholar
• 12. Hatipoglu M., Mutluoglu M., Turhan V., Uzun G., Lipsky B.A.Sevim E., Demiraslan H., Eryilmazh E., Ozuguz C., Memis A., Ay H.,Arda B., Uysal S., Motor V.K., Kader C., et al.: Causative pathogensREFERENCESand antibiotic resistance in diabetic foot infections: A prospectivemulti-center study. J. Diabetes Complications, 2016; 30: 910–916
  Google Scholar
• 13. International Best Practice Guidelines: Wound Managementin Diabetic Foot Ulcers. Wounds International, 2013. https://www.woundsinternational.com/resources/details/best-practice-guidelines-wound-management-diabetic-foot-ulcers
  Google Scholar
• 14. Kandemir O., Akbay E., Sahin E., Milcan A., Gen R.: Risk factorsfor infection of the diabetic foot with multi-antibiotic resistantmicroorganisms. J. Infect. 2007; 54: 439–445
  Google Scholar
• 15. Khan D.M., Moosabba M.S., Rao I.V.: Prevalence of diabeticfoot ulcer infections associated with Gram negative bacteria withspecial reference to drug resistant isolates. Int. J. Biomed. Res.,2016; 7: 765–770
  Google Scholar
• 16. Lipsky B.A., Berendt A.R., Cornia P.B., Pile J.C., Peters E.J., ArmstrongD.G., Deery H.G., Embil J.M., Joseph W.S., Karchmer A.W., PinzurM.S., Senneville E., Infectious Diseases Society of America: 2012Infectious Diseases Society of America clinical practice guidelinefor the diagnosis and treatment of diabetic foot infections. Clin.Infect. Dis., 2012; 54: e132–e173
  Google Scholar
• 17. Lipsky B.A., Berendt A.R., Deery H.G., Embil J.M., Joseph W.S.,Karchmer A.W., LeFrock J.L., Lew D.P., Mader J.T., Norden C., TanJ.S., Infectious Diseases Society of America: Diagnosis and treatmentof diabetic foot infections. Clin. Infect. Dis., 2004, 39: 885–910
  Google Scholar
• 18. Lipsky B.A., Senneville É., Abbas Z.G., Aragón-Sánchez J., DiggleM., Embil J.M., Kono S., Lavery L.A., Malone M., van Asten S.A.,Urbančič-Rovan V., Peters E.J., International Working Group on theDiabetic Foot (IWGDF): Guidelines on the diagnosis and treatmentof foot infection in persons with diabetes (IWGDF 2019 update).Diabetes Metab. Res. Rev., 2020; 36: e3280
  Google Scholar
• 19. Małecki R., Rosiński K., Adamiec R.: Etiological factors of infectionsin diabetic foot syndrome – attempt to define optimalempirical therapy. Adv. Clin. Exp. Med., 2014; 23: 39–48
  Google Scholar
• 20. Perim M.C., Borges J.C., Celeste S.R., Orsolin E.F., Mendes R.R.,Mendes G.O., Ferreira R.L., Carreiro S.C., Pranchevicius M.C.: Aerobicbacterial profile and antibiotic resistance in patients with diabeticfoot infections. Rev. Soc. Bras. Med. Trop., 2015; 48: 546–554
  Google Scholar
• 21. Ramakant P., Verma A.K., Misra R., Prasad K.N., Chand G.,Mishra A., Agarwal G., Agarwal A., Mishra S.K.: Changing microbiologicalprofile of pathogenic bacteria in diabetic foot infections:Time for a rethink on which empirical therapy to choose? Diabetologia,2011; 54: 58–64
  Google Scholar
• 22. Robson M.C., Heggers J.P.: Surgical infection. II. Theβ-hemolytic streptococcus. J. Surg. Res., 1969; 9: 289–292
  Google Scholar
• 23. Saseedharan S., Sahu M., Chaddha R., Pathrose E., Bal A., BhalekarP., Sekar P., Krishan P.: Epidemiology of diabetic foot infectionsin a reference tertiary hospital in India. Braz. J. Microbiol.,2018; 49: 401–406
  Google Scholar
• 24. Schaper N.C., van Netten J.J., Apelqvist J., Bus S.A., HinchliffeR.J., Lipsky B.A., IWGDF Editorial Board: Practical Guidelines on theprevention and management of diabetic foot disease (IWGDF 2019update). Diabetes Metab. Res. Rev., 2020; 36: e3266
  Google Scholar
• 25. Schultz G.S., Sibbald R.G., Falanga V., Ayello E.A., Dowsett C.,Harding K., Romanelli M., Stacey M.C., Teot L., Vanscheidt W.:Wound bed preparation: A systematic approach to wound management.Wound Repair Regen., 2003; 11: S1–S28
  Google Scholar
• 26. Singh S.K., Gupta K., Tiwari S., Shahi S.K., Kumar S., KumarA., Gupta S., Gupta S.K.: Detecting aerobic bacterial diversityin patients with diabetic foot wounds using ERIC-PCR: A preliminarycommunication. Int. J. Low Extrem. Wounds, 2009; 8:203–208
  Google Scholar
• 27. Smith K., Collier A., Townsend E.M., O’Donnel L.E., Bal A.M.,Buchter J., Mackay W.G., Ramage G., Williams C.: One step closerto understanding the role of bacteria in diabetic foot ulcers: Characterisingthe microbiome of ulcers. BMC Microbiol., 2016; 16: 54
  Google Scholar
• 28. Uçkay I., Aragón-Sánchez J., Lew D., Lipsky B.A.: Diabetic footinfections: What have we learned in the last 30 years? Review. Int.J. Infect. Dis., 2015; 40: 81–91
  Google Scholar
• 29. Yates C., May K., Hale T., Allard B., Rowlings N., Freeman A.,Harrison J., McCann J., Wraight P.: Wound chronicity, inpatient care,and chronic kidney disease predispose to MRSA infection in diabeticfoot ulcers. Diabetes Care, 2009, 32: 1907–1909
  Google Scholar

Full text