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 Table of Contents  
ORIGINAL ARTICLE
Year : 2013  |  Volume : 26  |  Issue : 1  |  Page : 49-53

Infection in diabetic foot


1 Department of Medical Microbiology and Immunology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of General Surgery, Faculty of Medicine, Menoufia University, Menoufia, Egypt
3 Department of Medical Microbiology and Immunology, Faculty of Medicine, King Abdul-Aziz University, Jeddah, Saudi Arabia

Date of Submission20-Feb-2013
Date of Acceptance12-Mar-2013
Date of Web Publication26-Jun-2014

Correspondence Address:
Ajlan E. Soma
MBBCh, Department of Medical Microbiology and Immunology, Faculty of Medicine, Menoufia University, Yassin Abdel Ghaffar Street of Gamal Abdel Nasser Street, Menuofia
Egypt
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Source of Support: None, Conflict of Interest: None


DOI: 10.7123/01.MMJ.0000429486.90373.5a

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  Abstract 

Objectives

The present study was carried out to determine the prevalence of aerobic and anaerobic pathogens in diabetic foot infections (DFIs), detect their susceptibility to different antimicrobial agents, investigate the microbiological profiles of DFIs in relation to different grades of Wagner classification, and assess the risk factors for DFIs.

Background

DFI is the most frequent reason for diabetes-related hospitalization. It develops because of several diabetes-related factors including arterial insufficiency, neuropathy, foot deformities, previous ulcers, previous amputation, and local trauma.

Materials and methods

The study was carried out on clinical specimens taken from 100 diabetic patients (50 patients had type I insulin-dependent diabetes mellitus (IDDM) and 50 patients had type II noninsulin-dependent diabetes mellitus (NIDDM) and 50 nondiabetic patients with foot infection during the period from May 2011 to July 2012. The specimens were cultured using aerobic and anaerobic microbiological techniques, and antibiotic susceptibility testing was performed according to the methods recommended by the Clinical and Laboratory Standards Institute (CLSI). Multidrug-resistant organisms were detected including oxacillin-resistant and vancomycin-resistant staphylococci and gram-negative bacilli extended-spectrum beta-lactamase producers.

Results

DFIs were polymicrobial in 76% of cases. Staphylococcus aureus was the most common aerobic isolate (17.6%) (including 74.4% methicillin resistant and 23.1% vancomycin resistant). Peptostreptococcus spp. were the most common anaerobic isolate (39.4%). Extended-spectrum β-lactamase production was detected in 53.4% of Gram-negative bacilli. About 62% of diabetic patients were infected with multidrug-resistant organisms. The risk factors for DFIs were duration of diabetes more than 1 year, random blood sugar of at least 200 mg/dl, trauma, previous ulcer and amputation, and comorbidities related to diabetes.

Conclusion

Imipenem was the most effective drug against all isolates. Effective glycemic control and educating patients on the prophylactic foot care are of key importance for decreasing DFIs.

Keywords: diabetic foot infection, multidrug-resistant organisms, polymicrobial, risk factors


How to cite this article:
Ahmed MB, Said AMI, Naira EA, Fatani AJ, Emad EM, Soma AE. Infection in diabetic foot. Menoufia Med J 2013;26:49-53

How to cite this URL:
Ahmed MB, Said AMI, Naira EA, Fatani AJ, Emad EM, Soma AE. Infection in diabetic foot. Menoufia Med J [serial online] 2013 [cited 2020 Feb 17];26:49-53. Available from: http://www.mmj.eg.net/text.asp?2013/26/1/49/135426


  Introduction Top


Diabetes mellitus is a serious public health problem and remains an important cause of morbidity and mortality worldwide 1. With the increase in the prevalence of diabetes mellitus, the incidence of diabetic foot infections (DFIs) has increased. It is estimated that 15% of patients with diabetes will develop a diabetic foot lesion during the course of their disease 2. Although 14–20% of patients with diabetic foot lesions will subsequently require an amputation, foot ulceration is the precursor to ∼85% of lower extremity amputations in individuals with diabetes 3. Furthermore, foot complications are the most frequent reason for hospitalization in patients with diabetes 4. DFIs develop because of several diabetes-related factors including arterial insufficiency, neuropathy (sensory, motor, and autonomic), foot deformities, previous ulcers, previous amputation, hyperglycemia, retinopathy, nephropathy, and long duration of diabetes 5. Severe DFIs usually yield polymicrobial isolates, whereas mild infections are frequently monomicrobial. In cases of a severe DFI, three to five organisms may be cultured 6. The Wagner classification classifies the severity and depth of tissue injury into five grades 7. In the superficial grades (Wagner I and II), aerobic bacteria are predominant pathogens, whereas anaerobic bacteria add up in Wagner grades III–V 8. Effective management of DFI requires appropriate antibiotic therapy, surgical drainage, debridement, resection of dead tissue, appropriate wound care, and correction of metabolic abnormalities 3.


  Materials and methods Top


In this study, 150 patients admitted to surgical wards or attending the outpatient clinics at Menoufia University Hospital and Sheben-Elkom Teaching Hospital with infected foot lesions were included. These patients were classified into three groups: the first group included 50 patients with type I diabetes, the second group included 50 patients with type II diabetes, and the third group included 50 nondiabetic patients. All patients were subjected to full assessment of personal and clinical history, and clinical, general, and local examination of the affected foot lesion. Tissue, pus, or swab samples were obtained from foot lesions. Parts of the collected specimens were placed in cooked meat broth for anaerobic cultures. All specimens were subjected to direct gram stain and primary aerobic cultures on nutrient agar, blood agar, mannitol salt agar, MacConkey agar, and Sabouraud’s dextrose agar for isolation of aerobic and facultative anaerobic pathogens. Specimens transported to the microbiology laboratory in cooked meat broth were cultivated on three selective media (Brucella blood agar supplemented with extra Gram-negative anaerobic selective supplement, extra nonspore forming anaerobic selective supplement, and Reinforced clostridial agar supplemented with neomycin supplement) and one nonselective brucella blood agar and immediately incubated at 37°C for 48 h anaerobically using a Gaspak anaerobic jar (BBL, Oxoid Limited, Basingstoke, Hampshire, England) (2.5 l capacity) and the AnaeroGen system (Oxoid Limited). Plates that showed no growth at 48 h were incubated for at least 5 days before discarding. The cooked meat broth tubes were incubated aerobically for 7 days and Gram stained daily. If bacterial cell types were observed that were not present on the primary plates, the broth was subcultured 9. Isolation and identification of the causative organisms were carried out according to the standard microbiological methods 10. Antimicrobial susceptibility of different isolates was determined using the disc diffusion method and interpreted according to the methods of the CLSI, the minimum inhibitory concentrations of vancomycin were determined for all staphylococcal isolates, and the phenotypic confirmatory double disk synergy test (DDST) was performed for the detection of extended-spectrum β-lactamase (ESβL) production in Gram-negative organisms detected by the screening disk diffusion test 11. Anaerobic antimicrobial susceptibility was determined using the broth disk elution method 12.


  Results Top


A total of 150 patients with infected foot lesions were included in this study; 50 patients had type I, 50 patients had type II diabetes mellitus, and 50 individuals were nondiabetics. Among the diabetic patients, 65 were men and 35 were women; the mean age of the patients was 47.1±1.0 years and the duration of foot ulcer was more than 1 month in 54% of diabetics. The risk factors for the development of DFIs are shown in [Table 1]. The number of patients graded by the Wagner classification is shown in [Figure 1]. The distribution of aerobic and anaerobic isolates from DFIs is shown in [Table 2] and the distribution of aerobic and anaerobic isolates by the Wagner classification is shown in [Table 3]. The antibiotic susceptibility results are presented in [Table 4]. Factors associated with the infection by multidrug-resistant organisms (MDROs) were the duration of ulcer more than 1 month, random blood sugar (RBS) at admission of at least 200 mg/dl, and Wagner grades III, IV, and V as presented in [Table 5].
Table 1: Risk factors for diabetic foot infection

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Table 2: Distribution of aerobic and anaerobic isolates from diabetic and nondiabetic patients with foot infection

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Table 3: Number of aerobic and anaerobic isolates from patients with various Wagner grades of diabetic foot infections

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Table 4: Antibiotic susceptibility of staphylococci and Gram-negative bacilli isolated from diabetic patients using the disk diffusion method

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Table 5: Relation of clinical data of diabetic patients multidrug-resistant organisms and nonmultidrug-resistant organisms to diabetic foot lesions

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Figure 1: Distribution of diabetic patients according to the Wagner classification.

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  Discussion Top


In the present study it was found that duration of diabetes was more than 1 year in 92% of patients, 76% of diabetics had been admitted to hospital with RBS of at least 200 mg/dl, trauma preceded DFI in 29% of patients, and 23% of diabetic patients had previous diabetic foot lesions. History of previous ulcer was more common (34%) in IDDM patients than NIDDM patients (12%) and 12% of our diabetic patients had previous amputations. Similar results were obtained by Ozer et al. 13 in Turkey; they found that in 92.3% of patients duration of diabetes was more than 1 year and 19.2% of DFIs were attending with trauma. Pappu et al. 14 in India found that 76% of diabetics had been admitted to hospital with RBS of at least 200 mg/dl. Mohanasoundaram 15 in India reported that 13% of diabetic patients had previous amputations. In terms of diabetes-associated comorbidities, the prevalence of hypertension was 57%, that of neuropathy was 62%, that of nephropathy was 17%, and that of retinopathy was 30%. Comparable results were obtained by Ozer et al. 13, who reported a 45% rate of hypertension and 32% rate of retinopathy, Gadepalli et al. 16 in India, who reported a 78.8% rate of hypertension, Mohanasoundaram 15, who found that 63% of diabetics had neuropathy, and Pappu et al. 14, who reported an 18% rate of nephropathy. Neuropathy, nephropathy, and retinopathy were more common in IDDM than NIDDM diabetes in our study. Longer duration of diabetes in IDDM patients may explain the more frequent complications.

In our study, 76% of cases had polymicrobial infections. This is in agreement with the result of Vimalin and Lali 17 in India, who reported that 75% of DFIs were polymicrobial. Staphylococcus aureus (17.6%) was the most common aerobic isolate, followed by Escherichia coli. Peptostreptococcus spp., which were the most common anaerobic isolate (39.4%), followed by Clostridium spp. (33.3%). Gram-positive cocci (staphylococci and streptococci) were predominant in Wagner grade I whereas Gram-negative bacilli were the most common isolates in other grades. Anaerobic isolation was found only in deep limb infections (in grades III, IV, and V) mixed with aerobic isolates in polymicrobial profiles. These findings are in agreement with those of Bengalorkar and Nagendra 5 and Lipsky et al. 6, who concluded that cellulitis of nonulcerated skin and superficial ulcers (often in Wagner grade I) are almost always caused by S. aureus and streptococci. Infection in deep or penetrating ulcers are usually mixed infections caused by Gram-positive cocci, Gram-negative bacilli, and obligate anaerobes, and are characterized by marked tissue necrosis and gangrene.

In the current study, S. aureus and coagulase-negative staphylococci (CoNS) isolated from diabetic lesions were highly sensitive to amikacin (100%), imipenem (92.3 and 100%, respectively), and cotrimoxazole (74.4% of S. aureus). This is in agreement with the results of Abdul Kadir et al. 18 in Brunei Darussalam, who reported high sensitivity of S. aureus to amikacin, imipenem (100% for each), and cotrimoxazole (90%). Also, oxacillin resistance was found in 74.4 and 54.5% of S. aureus and CoNS isolates from diabetic lesions. This is in agreement with the results of a study carried out in India by Zubair et al. 19, who found 71.4% were methicillin-resistant S. aureus. However, S. aureus and CoNS resistance to vancomycin was 23.1% and 18.2% using the MIC method in this study; comparable results were obtained by Hena and Growther 20 in India, who reported that vancomycin-resistant S. aureus was about 70.3% of all isolated S. aureus, and Al Benwan et al. 21 in Kuwait, who reported 100% sensitivity of S. aureus to vancomycin. All Gram-negative bacilli isolated from DFIs in the present study were highly sensitive to imipenem (98.3%) and amikacin (89.8%).This is similar to the results of El-Tahawy 22 in Saudi Arabia, who reported high sensitivity of Gram bacilli to imipenem (100%) and amikacin (89.9%). This study showed that ESβL producers by the disk diffusion test were 66.1% of the total Gram-negative bacilli isolated from diabetic patients, 60% of E. coli, 44.4% of Klebsiella spp., 75% of Citrobacter spp., 70.8% of Pseudomonas spp., and 66.7% of Proteus. Using the DDST, ESβL producers were 53.4% of the total isolated Gram-negative bacilli, 48.6% of E. coli, 33.3% of Klebsiella spp., 50% of Citrobacter spp., 58.2% of Pseudomonas spp., and 55.6% of Proteus. Comparable results were obtained in the study carried out in India by Zubair et al. 19, who reported that ESβL production by the disc diffusion screening test was 58% of gram-negative isolates, Pseudomonas aeruginosa (63.3%), Klebsiella spp. (59%), E. coli (54.6%), and Proteus vulgaris (44.6%). With the DDST, the percentage of ESβL production was 45.3% of Gram-negative isolates, P. aeruginosa (54%), Klebsiella spp. (41%), P. vulgaris (40%), and E. coli (38%). In this study, high sensitivity of the anaerobes isolated from DFIs was observed to imipenem (96.9%), ampicillin–sulbactam (93.9%), penicillin (90.9%), cefoxitin (84.8%), and clindamycin (81.8%), whereas low sensitivity was observed to metronidazole (60.6%). Similar results were obtained by Colayco et al. 9 in Philippine, who observed high sensitivity of the anaerobes isolated from DFIs to imipenem, ampicillin–sulbactam (96.6% for each), penicillin, cefoxitin (86.2% for each), and clindamycin (76%) and low sensitivity to metronidazole (52%). In the present study, MDROs were isolated from 62% of diabetic patients. A similar result (66.7%) was obtained by Khoharo et al. 23. Factors associated with the presence of infections by MDROs in our study were duration of ulcer more than 1 month that was observed in 78.5% of patients with MDROs infection. Also, RBS at admission of at least 200 mg/dl was found in 83.9% of patients with infection with MDROs and MDROs were more common in grade III (35.5%), grade IV(22.6%), and grade V patients (12.9%). Similar results were obtained in studies carried out in India by Zubair et al. 19, who reported a duration of ulcer of more 1 month in 79% of patients with infections by MDROs, RBS at admission of at least 200 mg/dl in 86% of patients with infections with MDROs, and Gadepalli et al. 16, who reported that MDROs were more common in Wagner grade III (50%), grade IV (34.5%), and grade V patients (15.5%).[23]

 
  References Top

1.Wild S, Roglic G, Green A, Sicree R, King H.Global prevalence of diabetes: estimates for the year 2000 and projections for 2030.Diabetes Care2004;27:1047–1053.  Back to cited text no. 1
    
2.Iversen MM, Tell GS, Riise T, Hanestad BR, Østbye T, Graue M, et al..History of foot ulcer increases mortality among individuals with diabetes: ten-year follow-up of the Nord–Trøndelag health study, Norway.Diabetes Care2009;32:2193–2199.  Back to cited text no. 2
    
3.Kirsner RS, William HH, Funnell MM.The standard of care for evaluation and treatment of diabetic foot ulcers2010The University of Michigan Health System’s Educational Services for Nursing and Barry University School of Pediatric Medicine; Michigan: The JB Ashtin Group;28.  Back to cited text no. 3
    
4.Alavi SM, Khosravi AD, Sarami A, Dashtebozorg A, Montazeri EA.Bacteriologic study of diabetic foot ulcer.Pak J Med Sci2007;23:681–684.  Back to cited text no. 4
    
5.Bengalorkar GM, Nagendra KT.Diabetic foot infections.Int J Biol Med Res2011;2:453–460.  Back to cited text no. 5
    
6.Lipsky BA, Berendt AR, Deery HG, Embil JM, Joseph WS, Karchmer AW, et al..Diagnosis and treatment of diabetic foot infections.Clin Infect Dis2004;39:885–910.  Back to cited text no. 6
    
7.Wagner FW Jr.The dysvascular foot: a system for diagnosis and treatment.Foot Ankle1981;2:64–122.  Back to cited text no. 7
    
8.Pathare NA, Bal A, Talvalkar GV, Antani DU.Diabetic foot infections: a study of microorganisms associated with the different Wagner grades.Indian J Pathol Microbiol1998;41:437–441.  Back to cited text no. 8
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9.Colayco CAS, Mendoza MT, Alejandria MM, Ang CF.Microbiologic and clinical profile of anaerobic diabetic foot infections.Philippine J Microbiol Infect Dis2002;31:151–160.  Back to cited text no. 9
    
10.Forbes BA, Sahm DF, Weissfeld AS.Overview of bacterial identification methods and srategies. Baily and Sott’s diagnostic microbiology2007.Philadelphia:Elsevier;216–248.  Back to cited text no. 10
    
11..Performance standards for antimicrobial susceptibility testing: twenty-first informational supplement2011.Pennsylvania:Clinical & Laboratory Standards Institute (CLSI).  Back to cited text no. 11
    
12.Baron EJ, Peterson LR, Fingold SM.Methods for testing antimicrobial effectiveness. Bailey & Scott’s diagnostic microbiology1990.Philadelphia:Elsevier;187–189.  Back to cited text no. 12
    
13.Ozer B, Kalaci A, Semerci E, Duran N, Davul S, Yanat AN.Infections and aerobic bacterial pathogens in diabetic foot.Afr J Microbiol Res2010;4:2153–2160.  Back to cited text no. 13
    
14.Pappu AK, Sinha A, Johnson A.Microbiological profile of diabetic foot ulcer.Calicut Med J2001;9:e2.  Back to cited text no. 14
    
15.Mohanasoundaram KM.The microbiological profile of diabetic foot infections.J Clin Diag Res2012;6:409–412.  Back to cited text no. 15
    
16.Gadepalli R, Dhawan B, Sreenivas V, Kapil A, Ammini AC, Chaudhry R.A clinico-microbiological study of diabetic foot ulcers in an Indian tertiary care hospital.Diabetes Care2006;29:1727–1732.  Back to cited text no. 16
    
17.Vimalin H, Lali G.Studies on bacterial infections of diabetic foot ulcer.Afr J Clin Exp Microbiol2010;11:146–149.  Back to cited text no. 17
    
18.Abdul Kadir KA, Satyavani M, Pande K.Bacteriological study of diabetic foot infections.Brunei Int Med J2012;8:19–26.  Back to cited text no. 18
    
19.Zubair M, Malik A, Ahmad J.Clinico-bacteriology and risk factors for the diabetic foot infection with multidrug resistant microorganisms in north India.Biol Med2010;2:22–34.  Back to cited text no. 19
    
20.Hena J, Growther L.Studies on bacterial infections of diabetic foot ulcer.Afr J Clin Exp Microbiol2011;11:146–149.  Back to cited text no. 20
    
21.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 Health2012;5:1–8.  Back to cited text no. 21
    
22.El Tahawy AT.Bacteriology of diabetic foot infections.Saudi Med J2000;21:344–347.  Back to cited text no. 22
    
23.Khoharo HK, Ansari S, Qurshi F.Diabetic foot ulcers: common isolated pathogens and in vitro antimicrobial activity.Prof Med J2009;16:53–60.  Back to cited text no. 23
    


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    Tables

  [Table 1], [Table 2], [Table 3], [Table 4], [Table 5]



 

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