|Year : 2014 | Volume
| Issue : 1 | Page : 28-34
Study of risk factors of diabetic foot ulcers
Nabil Abd El Fatah Al Kafrawy1, Ehab Ahmed Abd El-Atty Mustafa1, Alaa El-Din Abd El-Salam Dawood1, Osama Mohammed Ebaid2, Omnia Mahmoud Ahmed Zidane1
1 Department of Internal Medicine, Faculty of Medicine, Menoufia University, Menoufia, Egypt
2 Department of Radiology, Faculty of Medicine, Menoufia University, Menoufia, Egypt
|Date of Submission||18-Aug-2013|
|Date of Acceptance||24-Dec-2013|
|Date of Web Publication||20-May-2014|
Omnia Mahmoud Ahmed Zidane
Internal Medicine Department, Faculty of Medicine-Menoufia University, Shebin Al-Kom, Menoufia
Source of Support: None, Conflict of Interest: None
To study the risk factors for diabetic foot ulcers (DFUs) in Menoufia University Hospitals.
Problems associated with the diabetic foot are prevalent worldwide. DFUs contribute significantly toward the morbidity and mortality of patients with diabetes mellitus. This study was carried out to evaluate the risk factors for DFUs.
Patients and methods
One hundred patients with diabetic foot were enrolled and 50 patients had foot ulcers. All were subjected to the following: assessment of full history, physical examination including foot examination through peripheral pulses including Doppler examination of dorsalis pedis and posterior tibial arteries, sensations, reflexes and callus, and routine investigations including HbA1c, fasting, and 2 h postprandial blood glucose.
DFUs occurred mostly in patients who had had diabetes for a long duration more than 10 years (94%), smokers (50%), those with diabetic retinopathy (92%), those with previous ulcers (74%), those who had a previous amputation (42%), those with peripheral neuropathy assessed by [lost monofilament (100%), lost vibration sensation (100%), lost pinprick sensation (100%)], peripheral vascular disease assessed by [ankle brachial index≤0.9 (84%), Doppler examination detected ischemia (84%)], foot fissures (12%), foot callus (24%), foot deformities (36%), limited joint mobility (26%), dyslipidemia on the basis of elevated total cholesterol greater than 200 mg/dl (40%), and poor glycemic control on the basis of (hemoglobin A1C>7.5%). The types of ulcers were neuropathic (16%) and neuroischemic (84%). Age, sex, diabetic nephropathy, obesity detected by BMI, abnormal ankle reflexes, and elevated serum creatinine were not risk factors for DFUs.
Peripheral neuropathy, duration of diabetes, peripheral vascular disease, and poor glycemic control were significant predictors of DFUs.
Keywords: Diabetes mellitus, diabetic foot ulcer, peripheral neuropathy, peripheral vascular disease, retinopathy
|How to cite this article:|
Al Kafrawy NA, Mustafa EA, Dawood ADA, Ebaid OM, Ahmed Zidane OM. Study of risk factors of diabetic foot ulcers. Menoufia Med J 2014;27:28-34
|How to cite this URL:|
Al Kafrawy NA, Mustafa EA, Dawood ADA, Ebaid OM, Ahmed Zidane OM. Study of risk factors of diabetic foot ulcers. Menoufia Med J [serial online] 2014 [cited 2018 May 24];27:28-34. Available from: http://www.mmj.eg.net/text.asp?2014/27/1/28/132298
| Introduction|| |
Diabetic foot is a term for foot problems in patients with diabetes mellitus (DM) because of arterial abnormalities and diabetic neuropathy, as well as a tendency toward delayed wound healing, infection, or gangrene of the foot . Diabetic foot ulcer (DFU) is a major complication of DM and probably the major component of the diabetic foot. It occurs in 15% of all patients with diabetes and precedes 84% of all lower leg amputations . The principal contributory factors that might result in foot ulcer development are peripheral neuropathy, peripheral vascular disease, poor glycemic control, foot deformity, past foot ulcer history, previous amputation, visual impairment, diabetic nephropathy (especially patients on dialysis), and cigarette smoking . There are two main types of ulcers: neuropathic and ischemic. In patients with diabetes, pure ischemic ulcers are less common and the vast majority of ulcers are either pure neuropathic or mixed neuroischemic . The management of DFUs includes offloading the wound by using appropriate therapeutic footwear,  daily saline or similar dressings to provide a moist wound environment,  debridement when necessary, antibiotic therapy if osteomyelitis or cellulitis is present,  optimal control of blood glucose, evaluation and correction of peripheral arterial insufficiency, and wound coverage by cultured human cells  or heterogenic dressings/grafts. Application of recombinant growth factors  and hyperbaric oxygen treatments may also be beneficial at times, but only if arterial insufficiency is not present.
| Aim of work|| |
To study the risk factors for DFUs in Menoufia University Hospitals.
| Patients and methods|| |
This study was carried out on 100 diabetic patients with diabetic foot recruited from outpatient clinics and inpatient wards in Menoufia University Hospitals, Sheebin El-koom - Egypt, between April 2012 and April 2013. Their age ranged from 30 to 80 years. There were 49 men and 51 women in this study. The selected patients were subdivided into two groups (group I: 50 patients with DFU and group II: 50 patients without DFU). To carry out this research, the oral approval of the patients and approval of the ethics committee in the hospital were obtained.
Patients with diabetes, type 1 or type 2, with and without diabetic foot.
Patients with peripheral vascular diseases because of nondiabetic causes, patients with traumatic foot ulcers, and patients with joint diseases.
Patients were subjected to a thorough assessment of history, which included diabetic history (type of diabetes, duration, and treatment), macrovascular complications (coronary, cerebrovascular, and peripheral arterial diseases), microvascular complications (retinopathy and nephropathy), history of ulceration, amputation, vascular surgery, or angioplasty, history of smoking and history of hypertension, physical examination (anthropometric measurements such as BMI), blood pressure, foot examination that included neurological assessment for diabetic retinopathy through touch sensation, or sensory neuropathy that was assessed using a 10 g Semmes-Weinstein monofilament that was constructed to buckle when a 10g force is applied; loss of the ability to detect this pressure at one or more anatomic sites on the plantar surface of the foot has been associated with loss of large-fiber nerve function and the filament was pressed against several sites including (first, third, and fifth metatarsal heads and plantar surface of distal hallux) on each foot  Vibration sense was checked for neuropathies using a 128 Hz tuning fork,  patellar and ankle deep tendon reflexes, vascular assessment through palpation of dorsalis pedis and posterior tibial pulses, Doppler examination of dorsalis pedis and posterior tibial arteries with calculation of the ankle brachial index (ABI), dermatological assessment through color, temperature, hair, nails, and the presence of any skin lesions such as ulcers, corns, callus, fissures, and toe web macerations, and musculoskeletal assessment through joint flexibility, deformities such as hallux valgus, flat foot, toes deformities (hammer toe and claw toe), and Charcot's foot and gait assessment and footwear assessment.
Laboratory studies included the following: glycemic control was assessed by measuring HbA1C (glycosylated hemoglobin), fasting blood glucose and 2 h postprandial, lipid profile (serum cholesterol and triglycerides), serum creatinine, serum albumin, and urinalysis for the presence of albuminuria. Fundus examination was performed to check for retinopathy.
The data collected were tabulated and analyzed using statistical package for social science, version 17.0 on an IBM compatible computer.
Two types of statistics were calculated
0Number (No), percentage (%), mean (X), and standard deviation (SD) were determined.
Qualitative data were analyzed by χ2 and whenever one cell of the expected was equal to or less than 5, Fisher's exact test was used. Quantitative data were analyzed using the t-test (Student's test) for comparison of quantitative variables among two independent groups and the Mann-Whitney test (nonparametric test) for comparison between two groups that were not normally distributed.
Significance level (P) value: P value greater than 0.05 was considered nonsignificant (NS) and P value of up to 0.05 was considered significant (S).
| Results|| |
There were no significant differences between both groups in age, sex, and BMI. The mean duration of diabetes was significantly higher in the DFU patients group compared with diabetic patients without foot ulcer. The percentage of smokers was significantly higher in the DFU patients group (50%) compared with diabetic patients without foot ulcer (18%) [Table 1].
|Table 1: Comparison between diabetic patients with and without foot ulcer in terms of demographic data and laboratory tests|
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There was no significant difference between the two groups studied in serum creatinine, serum albumin, and serum triglycerides (P > 0.05). The mean serum total cholesterol, fasting, and 2H postprandial blood glucose and HbA1c were significantly higher in DFU patients compared with diabetic patients without foot ulcer [Table 1].
There was no significant difference between the groups studied in the presence of diabetic nephropathy (microalbuminuria), whereas the percentage of patients with diabetic retinopathy was significantly higher in the DFU patients group (92%) compared with diabetic patients without foot ulcer (76%) [Table 1].
[Table 2] shows that the percentage of patients with previous foot ulcer was significantly higher in the DFU patients group (74%) compared with diabetic patients without foot ulcer (4%). The percentage of patients with a previous lower limb amputation was significantly higher in the DFU patients group (42%) compared with diabetic patients without foot ulcer (0.0%). The percentage of patients with foot fissure, callus, deformities, and limited joint mobility was significantly higher among DFU patients compared with diabetic patients without foot ulcer.
|Table 2: Comparison between diabetic patients with and without foot ulcer in terms of diabetic foot examination|
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[Table 2] shows that monofilament sensation was lost in all diabetic patients with foot ulcer and only in 39 diabetic patients (78%) without foot ulcer. Vibration sensation was lost in all diabetic patients with foot ulcer and only in 32 diabetic patients (64%) without foot ulcer. Pinprick sensation was lost in all diabetic patients with foot ulcer and only in 39 diabetic patients (78%) without foot ulcer. The percentage of patients with lost monofilament sensation, vibration sensation, and pinprick sensation was significantly higher among DFU patients compared with diabetic patients without foot ulcer. There was no significant difference between the two groups studied in abnormal ankle reflexes.
[Table 3] shows that the mean ABI was 1.13 ± 0.15 in diabetic patients without foot ulcer and 0.81 ± 0.09 in diabetic patients with foot ulcer. It was significantly lower in DFU patients compared with diabetic patients without foot ulcer. Doppler examination detected lower limb ischemia in 42 diabetic patients (84%) with foot ulcer. No ischemia was detected by Doppler examination in any of the diabetic patients without foot ulcer. The number of patients with lower limb ischemia detected by Doppler was significantly higher among DFU patients compared with diabetic patients without foot ulcer.
In diabetic patients with foot ulcers, eight patients (16%) had neuropathic ulcer and 42 patients (84%) had mixed (neuroischemic) ulcer, whereas no pure ischemic ulcer was found during this study. The sites of foot ulcers were as follows: 12 patients (24%) with malleoli ulcers, 11 patients (22%) with marginal ulcers, 12 patients (24%) with heel ulcers, nine patients (18%) with sole ulcers, and six (12%) patients with ulcers of the toes. In total, 18 patients (36%) had right foot ulcers and 32 patients (64%) had left foot ulcers.
[Table 4] shows that age and sex were not significantly related to the risk of DFU (P > 0.05). The risk of DFUs was 16 times higher in patients who had a long duration of DM greater than 10 years [P < 0.001, odds ratio (OR) = 16.97], around two times more in smokers than nonsmokers (P < 0.001, OR = 1.94), patients who had diabetic retinopathy (P < 0.05, OR = 2.19), hypercholesterolemia (P < 0.05, OR = 2.36), five times more in patients who had previous foot ulcer (P < 0.001, OR = 4.45), two times more in patients who had lost monofilaments sensation (P < 0.001, OR = 2.28), in patients who had lost vibration sensation (P < 0.001, OR = 2.56), in patients who had lost pinprick sensation (P < 0.001, OR = 2.28), more in patients who had ABI of up to 0.9 (P < 0.001), five times more in patients who had foot deformities (P < 0.05, OR = 5.06), eight times more in patients who had limited joint mobility (P < 0.05, OR = 8.43), and two times more in patients who had HbA1c greater than 7.5% (P < 0.001, OR = 2.28).
|Table 4: Odds ratio of different parameters as risk factors for foot ulcer in diabetic patients|
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[Table 5] shows multivariate analysis of selected variables, which showed that the main risk factors for DFU were in order peripheral neuropathy (assessed by lost monofilaments sensation and lost vibration sensation), followed by duration of DM, peripheral vascular disease (assessed by ABI), and poor glycemic control (on the basis of HbA1c). The presence of diabetic retinopathy, elevated total cholesterol, and foot deformities was not significant.
|Table 5: Multivariate logistical regression analysis in diabetic patients with foot ulcer|
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| Discussion|| |
Foot ulcer is a disabling complication and not uncommon among patients with DM. The disability and possible progression to the loss (amputation) of digits and limbs make it a serious issue ,. The aim of the present study was to evaluate the risk factors for DFUs.
In the present study, there was no significant difference between diabetic patients with and without foot ulcer in terms of sex. This is similar to the study by Kumar et al.  who found no difference in the prevalence of DFU among male and female patients. Also, a study carried out in Jordan showed a prevalence of 5% of diabetes-related amputation among the studied population, where sex was not a significant risk factor .
In contrast, several studies have shown that male sex was identified as a risk factor in a cross-sectional study carried out by Frykberg et al.  Also, Moss et al.  found that male sex was a significant factor in predicting amputation.
In general, the prevalence of peripheral vascular disease and sensory neuropathy is lower in women compared with men with diabetes ,. Numerous factors may play a role in the effect of sex on diabetic foot lesions. These may include activity level, smoking, hormonal differences, degree of compliance, level of denial, the prevalence and severity of vascular disease, and neuropathy ,.
In the current study, we found that the mean duration of diabetes was significantly higher in DFU patients compared with non-DFU patients (P < 0.001) and patients with more than 10 years of DM duration showed 16.97-fold increases in the prevalence of DFU compared with patients with less than 10 years of DM duration. In agreement with our results, Reiber  showed a six-fold increase in the risk of DFU in patients with 20 years or more of DM compared with patients with a shorter duration of DM. This is in agreement with other studies that showed that long duration of diabetes was the main factor causing DFUs ,,,,. This is most likely because of other risk factors such as peripheral neuropathy and peripheral vascular disease developing with time .
In our study, there was no significant difference between diabetic patients with and without foot ulcer in terms of BMI. This is in agreement with Mantely et al. , who found no association between the BMI and the risk for DFU. However, evidence from a number of studies shows an association between greater body weight and higher risk for foot ulceration ,. This may be related to the effect of body weight on the planter pressure, although evidence to suggest such an association is not consistent .
In this study, we found that smoking was another significant risk factor for DFU. In agreement with our results, Moss et al.  found that smoking was predictive of foot ulceration and amputation. Diabetic foot ulcerations were more common in younger patients who smoked than in nonsmokers, but this was not the case in elderly patients. Nevertheless, smoking is a strong risk factor for peripheral vascular disease (PVD), which is associated with DFU . This observation was also supported by other studies ,. In contrast to our results, Coppini et al.  failed to show any association between foot complications and smoking. Several other studies have failed to show an association between smoking and amputations as Selby et al.  and Letho et al. .
In the present study, it was found that previous foot ulcer and previous lower limb amputation were significantly related to DFU. Previous studies have shown that a history of ulcer ,,,,, and previous lower limb amputation ,,,,,, increase the risk for further lesions. This may be attributed to previous foot ulcer and amputation leading to loss of protective sensation (peripheral neuropathy) .
In the current study, we found that peripheral neuropathy (assessed by insensitivity to 10 g Semmes-Weinstein monofilament, lost vibration sensation, and pinprick sensation) was the main risk factor for DFU. Previous studies have shown that peripheral neuropathy was a strong independent risk factor for the development of DFUs ,,,,; also, our observation of inability to feel a 5.07 Semmes-Weinstein monofilaments was confirmed by other studies [39,44]. This was as attributed to the fact that patients with neuropathy may have sensory, motor, and/or autonomic peripheral neuropathy. Sensory neuropathy leads to loss of protective function and loss of recognition of the consequence of repetitive trauma. Neuropathy, including motor neuropathy, results in the typical foot deformities, and including Charcot foot, which increases pressure load on bony prominences. Finally, autonomic neuropathy leads to excessive callus formation, which is also a risk factor for development of DFU .
In the present study, we found that peripheral vascular disease was a significant risk factor for DFU. This was supported by other studies ,,, which showed that peripheral vascular disease is a major contributing factor toward the development of foot ulcers. A previous study has also shown that absent foot pulses were significant risk factors for ulceration . This may be attributed to the fact that patients with diabetes and severe peripheral arterial disease have increased susceptibility to sudden ischemia resulting from arterial thrombosis, which may lead to critical limb ischemia and may increase the risk of ulcer and amputation . In contrast, Alex et al.  showed that absent pulse was a nonsignificant risk factor for ulceration and Dinh et al.  showed that an abnormal ABI was a nonsignificant risk factor for ulceration.
In the current study, it was found that poor glycemic control was a significant risk factor for DFU. These findings were confirmed by other studies ,, that showed that poor glycemic control was the main factor causing diabetic foot problems. Previous studies have also shown that HbA1c was a contributory factor for DFU ,,,. This may be because of hyperglycemia, which has been considered a risk factor for the development of DFUs because of its contribution toward the development of peripheral neuropathy and microvascular complications .
In the present study, we found patients who had retinopathy, foot fissures, callus, foot deformities, and limited joint mobility to be at increased risk. Previous studies supported our observation on retinopathy, ,,, presence of callus, , foot deformities, ,,,, and limited joint mobility . In contrast, Alex et al.  showed that foot deformity was a nonsignificant risk factor for foot ulcer.
In the current study, diabetic nephropathy was not a risk factor for DFU. This is similar to a study carried out at the Texas Diabetes Institute and The University of Texas Health Science Center Clinics at San Antonio, USA. They concluded that microvascular disease (nephropathy and retinopathy) was not a significant risk factor for ulceration in either the univariate or the multivariate analysis . In contrast, Fernando et al.  confirmed that patients at all stages of diabetic nephropathy, even microalbuminuria, have an increased risk of foot ulceration.
| Conclusion|| |
Our study showed that the significant predictive factors for DFU development were peripheral neuropathy, duration of diabetes, peripheral vascular disease, and poor glycemic control in order. Most of the risk factors related to DFU are correctable or at least controllable, with a huge opportunity for early prevention and treatment, with the subsequent reduction in patients suffering from DFU and its sequel of amputation.
| Acknowledgements|| |
Conflicts of interest
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[Table 1], [Table 2], [Table 3], [Table 4], [Table 5]