Microbial Profile and Antibiotic Susceptibility Pattern in Diabetic Patients with Mild, Moderate, and Severe Foot Infections in Tehran

Document Type : Original Articles

Authors

1 Department of Microbiology, School of Medicine, Tehran University of Medical Sciences, Tehran, Iran

2 Endocrinology and Metabolism Research Center, Endocrinology and Metabolism Clinical Science Institute, Tehran University of Medical Sciences, Tehran, Iran

3 Medical Mycology and Bacteriology Research Center, Kerman University of Medical Sciences, Kerman, Iran

Abstract

It is estimated that 10-25% of diabetic patients will encounter diabetic foot ulcers (DFU) during their lifetime. This study evaluated the microbiology of DFUs and determined the antibiotic resistance pattern of bacterial isolates based on the severity of wounds and infections in different grades of ulcer. The specimens were collected from115 diabetic foot infections (DFI) deep tissue by needle aspiration and biopsy. The aerobic and anaerobic cultures and antimicrobial susceptibility testing were carried out. The presence of resistance genes including Metallo-beta-lactamases (MBL), extended-spectrum β-lactamase (ESBL), ermA, ermC, and mecA was also determined. A total of 222 microorganisms were isolated. The prevalence of poly-microbial infections was 69.6%. Bacterial isolates comprised 64.2% Gram-positive bacteria (GPB), 33.5% Gram-negative bacteria (GNB), and five isolates of anaerobic bacteria were also detected. The most prevalent GPB and GNB were Staphylococcus spp. (52.2%) and Escherichia coli (33.3%), respectively. The prevalence of poly-microbial infections and GNB was positively associated with increased grades of Wagner and IDSA classifications. Among Staphylococcus aureus isolates, resistance to clindamycin (73.5%), ciprofloxacin (70.6%), and erythromycin (70.6%) were noticeable. GNB was also highly resistant to cephalosporins and ciprofloxacin. ESBL genes were detected in approximately 40% of isolates of Enterobacteriaceae. The prevalence of Erma, ermC, and mecA genes in S. aureus isolates were 8.8%, 32.3%, and 14.7%, respectively. In conclusion, our data suggest that GPBs are the most common isolates from DFIs. Furthermore, with the development of wounds and infection, the prevalence of GNB in DFIs are increased.

Keywords

Main Subjects


  1. Henig O, Pogue JM, Martin E, Hayat U, Ja’ara M, Kilgore PE, et al. The Impact of Multidrug-Resistant Organisms on Outcomes in Patients With Diabetic Foot Infections. Open Forum Infect Dis. 2020;7(5):161.
  2. Macdonald KE, Jordan CY, Crichton E, Barnes JE, Harkin GE, Hall LM, et al. A retrospective analysis of the microbiology of diabetic foot infections at a Scottish tertiary hospital. BMC Infect Dis. 2020;20(1):1-7.
  3. Ahmad J. The diabetic foot. Diabetes Metabolism Syndrome. 2016;10(1):70-8.
  4. 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(12):e132-e73.
  5. Al Ayed MY, Ababneh M, Alwin Robert A, Alzaid A, Ahmed RA, Salman A, et al. Common pathogens and antibiotic sensitivity profiles of infected diabetic foot ulcers in Saudi Arabia. Int J Low Extrem Wounds. 2018;17(3).
  6. Lavery LA, Ryan EC, Ahn J, Crisologo PA, Oz OK, La Fontaine J, et al. The Infected Diabetic Foot: Re-evaluating the Infectious Diseases Society of America Diabetic Foot Infection Classification. Clin Infect Dis.2020;70(8):1573-9.
  7. Wu M, Pan H, Leng W, Lei X, Chen L, Liang Z. Distribution of microbes and drug susceptibility in patients with diabetic foot infections in Southwest China. J Diabetes Res. 2018;2018.
  8. Machado C, Teixeira S, Fonseca L, Abreu M, Carvalho A, Pereira MT, et al. Evolutionary trends in bacteria isolated from moderate and severe diabetic foot infections in a Portuguese tertiary center. Diabetes Metab Syndr. 2020;14(3):205-9.
  9. Sadeghpour Heravi F, Zakrzewski M, Vickery K, G Armstrong D, Hu H. Bacterial diversity of diabetic foot ulcers: current status and future prospectives. Clin Med (Lond). 2019;8(11):1935.
  10. Saeed K, Esposito S, Akram A, Ascione T, Bal AM, Bassetti M, et al. Hot topics in diabetic foot infection. Int J Antimicrob Agents. 2020;55(6):70.
  11. Lipsky BA, Senneville É, Abbas ZG, Aragón‐Sánchez J, Diggle M, Embil JM, et al. Guidelines on the diagnosis and treatment of foot infection in persons with diabetes (IWGDF 2019 update). Diabetes Metab Res Rev. 2020;36:e3280.
  12. Martinengo L, Olsson M, Bajpai R, Soljak M, Upton Z, Schmidtchen A, et al. Prevalence of chronic wounds in the general population: systematic review and meta-analysis of observational studies. Ann Epidemiol.2019;29:8-15.
  13. Institute CaLS. CLSI, Performance Standards for Antimicrobial Susceptibility Testing, 29th ed, CLSI Supplement M100, Wayne, PA. 2019.
  14. Magiorakos A-P, Srinivasan A, Carey Rt, Carmeli Y, Falagas Mt, Giske Ct, et al. Multidrug-resistant, extensively drug-resistant and pandrug-resistant bacteria: an international expert proposal for interim standard definitions for acquired resistance. Clin Microbiol Infect.2012;18(3):268-81.
  15. Neyestanaki DK, Mirsalehian A, Rezagholizadeh F, Jabalameli F, Taherikalani M, Emaneini M. Determination of extended spectrum beta-lactamases, metallo-beta-lactamases and AmpC-beta-lactamases among carbapenem resistant Pseudomonas aeruginosa isolated from burn patients. Burns. 2014;40(8):1556-61.
  16. Mirsalehian A, Kalantar-Neyestanaki D, Taherikalani M, Jabalameli F, Emaneini M. Determination of carbapenem resistance mechanism in clinical isolates of Pseudomonas aeruginosa isolated from burn patients, in Tehran, Iran. Clin Epidemiol Glob Health. 2017;7(3):155-9.
  17. Motallebi M, Jabalameli F, Beigverdi R, Emaneini M. High prevalence of direct repeat unit types of 10di, 8 h and 8i among methicillin resistant Staphylococcus aureus strains with staphylococcal cassette chromosome mec type IIIA isolated in Tehran, Iran. Antimicrob Resist Infect Control. 2019;8(1):50.
  18. Arias M, Hassan-Reshat S, Newsholme W. Retrospective analysis of diabetic foot osteomyelitis management and outcome at a tertiary care hospital in the UK. PloS One. 2019;14(5).
  19. 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;18(2):122-8.
  20. Najari HR, Karimian T, Parsa H, QasemiBarqi R, Allami A. Bacteriology of moderate-to-severe diabetic foot infections in two tertiary hospitals of Iran. Foot. 2019;40:54-8.
  21. Hitam SAS, Asma’Hassan S, Maning N. The Significant Association between Polymicrobial Diabetic Foot Infection and Its Severity and Outcomes. Malays J Med Sci. 2019;26(1):107.
  22. Liu L, Li Z, Liu X, Guo S, Guo L, Liu X. Bacterial distribution, changes of drug susceptibility and clinical characteristics in patients with diabetic foot infection. Exp Ther Med. 2018;16(4):3094-8.
  23. 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.
  1. Sánchez-Sánchez M, Cruz-Pulido WL, Bladinieres-Cámara E, Alcalá-Durán R, Rivera-Sánchez G, Bocanegra-García V. bacterial prevalence and antibiotic resistance in clinical isolates of diabetic foot ulcers in the Northeast of Tamaulipas, Mexico. Int J Low Extrem Wounds. 2017;16(2):129-34.
  2. Ghotaslou R, Memar MY, Alizadeh N. Classification, microbiology and treatment of diabetic foot infections. J Wound Care. 2018;27(7):434-41.
  3. Nikoloudi M, Eleftheriadou I, Tentolouris A, Kosta OA, Tentolouris N. Diabetic foot infections: update on management. Curr Infect Dis. 2018;20(10):1-11.
  4. Giurato L, Meloni M, Izzo V, Uccioli L. Osteomyelitis in diabetic foot: a comprehensive overview. World J Diabetes. 2017;8(4):135.
  5. Berendt A, Peters E, Bakker K, Embil J, Eneroth M, Hinchliffe R, et al. Diabetic foot osteomyelitis: a progress report on diagnosis and a systematic review of treatment. Diabetes Metab Res Rev. 2008;24(S1):S145-S61.
  6. Arias M, Hassan-Reshat S, Newsholme W. Retrospective analysis of diabetic foot osteomyelitis management and outcome at a tertiary care hospital in the UK. PloS One. 2019;14(5):e0216701.
  7. Lauri C, Leone A, Cavallini M, Signore A, Giurato L, Uccioli L. Diabetic foot infections: the diagnostic challenges. J Clin Med. 2020;9(6):1779.
  8. Rastogi A, Sukumar S, Hajela A, Mukherjee S, Dutta P, Bhadada SK, et al. The microbiology of diabetic foot infections in patients recently treated with antibiotic therapy: a prospective study from India. J Diabetes Complicat 2017;31(2):407-12.
  9. Senneville É, Lipsky BA, Abbas ZG, Aragón‐Sánchez J, Diggle M, Embil JM, et al. Diagnosis of infection in the foot in diabetes: a systematic review. Diabetes Metab Res Rev. 2020;36:e3281.
  10. Sen P, Demirdal T, Emir B. Meta‐analysis of risk factors for amputation in diabetic foot infections. Diabetes Metab Res Rev. 2019;35(7):e3165.

34.          Stacey HJ, Clements CS, Welburn SC, Jones JD. The prevalence of methicillin-resistant Staphylococcus aureus among diabetic patients: a meta-analysis. Acta Diabetol. 2019;56(8):907-21.