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Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes
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Primary Care Diabetes journal homepage: http://www.elsevier.com/locate/pcd
Original research
Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes S.H. Assaad-Khalil a,∗ , A. Zaki b , A. Abdel Rehim a , M.H. Megallaa a , N. Gaber a , H. Gamal a , K.H. Rohoma a a b
Department of Internal Medicine (Unit of Diabetes), Alexandria University, Alexandria, Egypt Department of Biostatistics, Alexandria University, Alexandria, Egypt
a r t i c l e
i n f o
a b s t r a c t
Article history:
Introduction: Multiple pathologies including diabetic neuropathy, peripheral vascular disease
Received 10 June 2012
(PVD) and infection contribute to lower extremities amputation in diabetes.
Received in revised form
Aim: We examined the prevalence of diabetic foot problems and related risk factors in Egypt.
30 August 2014
Subjects and methods: Between July 2008 and December 2009, 1000 male and 1000
Accepted 31 October 2014
female consecutive adult patients with diabetes (≥18-year-old) attending the Alexan-
Available online xxx
dria University Diabetic Foot Screening Clinic were surveyed for history/presence of foot ulcers and/or amputations, skin/nail changes, joint mobility, sensory neuropathy (10 g-
Keywords:
Semmes–Weinstein Monofilament) and peripheral vascular disease (PVD) using Ankle
Risk factors
Brachial Index (ABI).
Prevalence
Results: The majority of patients had type 2 diabetes (96.75%) with a mean age of 57.30 ± 10.47
Diabetic foot
years and a mean disease duration of 11.76 ± 8.26 years. The mean body mass index was
Egypt
32.84 ± 6.31 kg/m2 with 29.55% being current or ex-smokers. In these subjects, 4.4% had a past history of non-traumatic amputation (male:female: 6.2% vs. 2.6%, p < 0.001); 6.1% had past history (10.3% vs. 7%, p = 0.009) and 8.7% had active foot ulceration (8.1% vs. 4.1% p < 0.001) with a male preponderance. The prevalence of sensory neuropathy was 29.3% (M:F: 30.7%: 27.9%) and peripheral vascular disease (PVD) was 11% (M:F 11.8%:10.2%). Diabetic foot complications were associated with disease duration (p < 0.001), history of coronary artery disease (p = 0.001), stroke (p = 0.009), PVD (p < 0.001), laser photocoagulation (p < 0.001), sensory neuropathy (p < 0.001) and renal replacement therapy (p < 0.001). On multivariate analysis, diabetes duration, foot fissures, Charcot’s foot, limited joint mobility, PVD and sensory neuropathy remained independently associated with diabetic foot disorders. Conclusion: In Egypt, a mosaic of risk factors contributes to the high prevalence of diabetic foot disease in type 2 diabetes. These findings call for regular assessment of vascular, neuropathic and skin status to prevent these serious foot complications. © 2014 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.
∗
Corresponding author. Tel.: +20 1222197789; fax: +20 34833321. E-mail address: [email protected] (S.H. Assaad-Khalil).
http://dx.doi.org/10.1016/j.pcd.2014.10.010 1751-9918/© 2014 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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1.
Introduction
The diabetic foot syndrome encompasses a number of pathologies, including diabetic neuropathy, peripheral vascular disease, Charcot’s neuroarthropathy, foot ulceration, osteomyelitis, and the potentially preventable end point, amputation [1]. Subjects with diabetic foot problems are also likely to harbor other associated complications of diabetes such as nephropathy, retinopathy, ischemic heart disease and cerebrovascular disease [2]. The burden of diabetic foot disease is set to increase in the future since the contributory factors to foot disease, such as peripheral neuropathy and vascular disease, are present in more than 10% of people at the time of diagnosis of type 2 diabetes [3]. The annual populationbased incidence of foot ulceration is approximately 1–4% [4], and the prevalence ranges from 4% to 10% which suggests that lifetime risk can range from 15% to as high as 25% [5]. Diabetic foot ulcers/infections negatively impact quality of life (QOL), increase morbidity and mortality and also incur a substantial economic burden for society, patients and their families [6]. Amputation is a serious consequence of diabetes. Lower limb amputation is performed 10–30 times more frequently among diabetic than among general population [7]. Every 30 s, somewhere in the world, a lower limb is lost as a complication of diabetes [8]. One report noted that more than 80% of non-traumatic lower extremity amputations (LEAs) are performed in diabetic patients [9]. and more than 85% of these were precipitated by a foot ulcer that subsequently progressed to a severe infection [7]. Individuals are at high risk for amputation of the contralateral limb if they have already undergone amputation of one limb. Furthermore, 30–50% of first-episode amputations will progress to subsequent amputations within 1–3 years. Amputation carries with it a significantly elevated mortality at follow-up, ranging from 13% to 40% at 1 year to 39–80% at 5 years [10]. The study of the epidemiology of diabetic foot disease has been beset by numerous problems related to diagnostic tests and population selection. Few studies have reported the prevalence of diabetic foot disorders in Egypt. The aim of this work was to detect the prevalence of diabetic foot problems among Egyptian population, related risk factors and the associated diabetes complications among patients with ulceration or amputation.
2.
Methods
2.1.
Research design
This is a cross sectional study to estimate the prevalence of diabetic foot complications among attendants of the Diabetic Foot Screening Clinic (DFSC) in Alexandria. A nested case control study was undertaken to assess risk factors for the development of diabetic foot complications.
2.2.
Setting and study population
Alexandria Main University Hospital runs two diabetes clinics, a general diabetes clinic and a Diabetic Foot Screening Clinic (DFSC). The later was recently established by a fund from the IDF BRIDGES to be a screening and a preventive center in addition to provision of primary foot care services like callus debridement, nail cutting, treatment of foot infections etc. All patients attending the general diabetes clinic (whether from Alexandria or the surrounding governorates) were given appointments to attend the diabetic foot clinic (without prior selection). Response rate was high (93.4%) as we were the only provider of foot care service in that region of the country, so the attendance rate was 4–6 patients per day amounting to around one thousand patients per year. Enrolment in the diabetic foot registry was done based on the order of patient attendance. Professors, consultants, specialist, residents, and house officers, together with trained nurses and health workers participated in the clinic.
2.3.
Sample size
According to previous studies we expect the average prevalence of diabetic foot complications to be around 6% in adult males and females. To achieve a study power equal to 80%, at confidence level 95%, and with precision ±2 around our estimate, the calculated sample size was found to be equal to 958. Accordingly, we planned to recruit 1000 male and 1000 female consecutive diabetic patients from among attendants of the DFSC for routine check up during the period from July 2008 to December 2009. Only Patients aged above 18 years old who had been already diagnosed with diabetes according to WHO criteria were eligible.
2.4.
Data collection
Study participants had a face-to-face interview with one the physicians to collect data using a standardized questionnaire [11] about the following variables: Demographic characteristics, duration of DM, symptoms of neuropathy using the diabetic neuropathy symptom (DNS) score [12], smoking habits, past history of related co morbidities like hypertension, coronary heart diseases, cerebrovascular stroke, claudication, revascularization, renal transplantation or dialysis and laser photocoagulation. All participants were clinically examined. The general clinical examination was carried by physicians (consultant, specialist, or resident) and included measurement of blood pressure, recording of the patient weight and height with calculation of body mass index (BMI). The feet were thoroughly examined for the presence of foot ulcers and/or amputations. Foot deformities including halux valgus, hammer/claw toe, flat foot and Charcot’s foot. The skin of the foot was also assessed for presence of callus, corns, fissuring and presence of toe web macerations. The foot nails were examined to detect presence of nail dystrophies, ingrowing nails & onychomychosis. Foot joint mobility was assessed to detect limited joint mobility which was defined as less than 50◦ of non-weight bearing passive dorsiflexion of the hallux.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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The neurological status of the foot was assessed using 10 g-Semmes–Weinstein Monofilament examination. A 5.07 Semmes–Weinstein nylon monofilament was employed to apply a consistent 10 g force on 9 different sites; planter surface of the first, third and fifth toes; under head of first, third and fifth metatarsal bones; planter surface of the mid-foot; heel and dorsal space between the first and second toe. The sensation of pressure using the buckling 10-g monofilament was first demonstrated to the patient on a proximal site. Then with the patients unable to see their feet, the monofilament was placed on the plantar surface of the foot at right angles to the skin and the pressure increased until the filament buckled. The patients were asked to say “yes” when they felt something. Areas of callus were avoided. A foot is classified to have loss of protective sensation or sensory neuropathy when less than seven sites were felt by the patient. A foot is classified as normal if seven or more sites were felt by the patient. Peripheral vascular status of the foot was assessed by measuring Ankle Brachial Index (ABI) for dorsalis pedis & posterior tibial arteries of both feet. Ankle pressures were measured using a standardized Doppler ultrasonic device (5 MHz; Nicolet Elite 200 R, VIASYS Healthcare Inc., Madison, WI, USA). ABI was calculated as the ratio of the higher of the two systolic pressures (from posterior tibial and dorsalis pedis) at the ankle to the higher reading of the right and left brachial artery pressures. Pressures in each leg were measured and ABI was calculated separately for each leg. In the case of a missing ABI value in one leg, the value from the other was used, and likewise for missing brachial artery pressure values in one arm. Peripheral arterial disease (PAD) was defined as an ABI of ≤0.9 in at least one leg. The lower ABI between the two legs was used to define PAD. The patient was considered to have diabetic foot disorder if he has any of the following disorders attributed to his diabetic condition: amputation, active foot ulcer or previous foot ulcer. Individuals with foot disorders were assigned to only one of the mutually exclusive groups. The diabetic patient with amputation was assigned only to the amputation group whether or not he had active ulcer or history of previous ulcer. An individual with diabetic active foot ulcer and not having amputation was assigned only as having active foot ulcer whether or not he had history of previous ulcer. The patients assigned to the group with previous ulcer, gave this history but did not suffer amputation or current active foot ulcer.
2.5.
3
Association between co morbidities, skeletal deformities and foot joints mobility and the development of diabetic foot disorders was tested using Chi square test. All risk factors significantly associated with diabetic foot complications (p < 0.05) in the bivariate analysis were included as independent variables in a multivariate logistic model with diabetic foot complication as an outcome variable. The adjusted OR with 95%CI for each risk factor was calculated controlling for the effect of other co variables.
3.
Results
The study sample included 1000 males and 1000 females, the majority were type 2 diabetes (96.75%). The mean age was 57.30 ± 10.47 years and the mean known duration of diabetes was 11.76 ± 8.26 years. The mean BMI of our patients was 32.84 ± 6.31 kg/m2 . The habit of smoking (current/ex-smoker) was present in 29.55% of the total population. The prevalence of non-traumatic amputation was 4.4% (6.2% among males and 2.6% among females),with statistical significance (p < 0.001). Active foot ulceration was identified in 6.1% (8.1% among males, 4.1% among females),with statistical significance (p < 0.001). While the prevalence of past foot ulceration was 8.7%(10.3% among males and 7% among females, with statistical significance (p = 0.009). Therefore the overall prevalence of ulceration and amputation was 11.85%. The overall prevalence among males was higher than that among females (14.1% and 9.7%, respectively) with a significant relationship (p = 0.002). Diabetic foot disorders, was defined by the presence of non-traumatic foot amputation or current active foot ulcer or history of previous foot ulcer. There was a statistically significant trend for the increase in the prevalence of diabetic foot disorders with the increase of the duration of DM among our study population (p < 0.001) as shown in Fig. 1. There was a significant association between the prevalence of diabetic foot disorders (DFD) and both macrovascular and microvascular complications (Table 1). There was a statistically significant relationship between the presence of several dermatological examination findings and the prevalence of diabetic foot disorders. These findings include foot fissures (17.53% in patients with fissures vs. 11.3% in patients did not have fissures, p = 0.011), foot callus (14.76%
Ethical submission
The study was reviewed and approved by the Institutional Review Board/Research Ethics Committee of the Faculty of Medicine, Alexandria University, Alexandria; Egypt.
2.6.
Statistical analysis
Statistical analysis was performed using SPSS version 18.0 (SPSS Inc, Chicago, Illinois, USA). Quantitative variables like age, BMI and duration of diabetes were presented as mean ± SD, while qualitative variables like sex, smoking (current/ex-smoker/non smokers), frequency of different diabetic foot disorder were presented as percentage.
Fig. 1 – Prevalence of diabetic foot complications in the study population presented according to the duration of diabetes.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Table 1 – Association between co morbidities and diabetic foot disorders in 2000 diabetic patients. Comorbiditiy
Hypertension
Coronary artery disease
Cerebrovascular stroke
Claudication
Revascularization
Free f
Yes (N = 1024) No (N = 976)
819
Yes (N = 421) No (N = 1579)
310
Yes (N = 45) No (N = 1955) Yes (N = 213) No (N = 1787) Yes (N = 25) No (N = 1975)
Renal transplantation or dialysis.
Yes (N = 69) No (N = 1931)
Laser photocoagulation
Yes (N = 250) No (N = 1750)
∗
798
1307
32 1585
159 1458
7 1610
69 136
136 1481
p-Value*
Diabetic foot disorders History of foot ulcer n = 173
Active foot ulcer n = 122
Amputation n = 88
92 8.98% 81 8.30%
56 5.47% 66 6.76%
57 5.57% 31 3.18%
0.198
52 12.35% 121 7.66%
33 7.84% 89 5.64%
26 6.16% 62 3.93%
0.001*
7 15.56% 166 8.49%
5 11.11% 117 5.98%
1 2.22% 87 4.45%
0.009*
27 12.68% 146 8.17%
13 6.10% 109 6.10%
14 6.57% 74 4.14%
0.005*
7 28% 166 8.41%
6 24% 116 5.87%
5 20% 83 4.20%
<0.001*
11 15.94% 162 8.39%
7 10.14 115 5.96%
6 8.70% 82 4.25%
0.001*
51 20.4% 122 6.97%
33 13.2% 89 5.09%
30 12% 58 3.31%
<0.001*
indicates a statistically significant difference.
in patient with vs. 10.92% in patient without callus, p = 0.021). On the other hand, the presence of corns or toe web maceration did not show significant relation with the prevalence of diabetic foot disorders. In our study, the prevalence of peripheral diabetic neuropathy among the total study population was 29.3%. (30.7% in males and 27.9% in females with statistical significance; p = 0.168). The presence of diabetic peripheral neuropathy was defined based on the inability to perceive 2 or more sites out of 9 when using the 10 g Semmes–Weinstein monofilament. Peripheral diabetic neuropathy was found to be a highly statistically significant risk factor for the presence of diabetic foot complications. The prevalence of PAD was (11%) among the total study population. The prevalence was (11.8%) among males and (10.2%) among females. PAD was defined based on the assessment of Ankle–Brachial Index (ABI) <0.9. Presence of PAD showed a high statistical significance with the occurrence of diabetic foot amputation and ulceration (27.9% in patients with ulceration and amputation vs. 11.9% diabetics without ulceration and amputations, O.R. = 2.65) (p < 0.001).
The prevalence of active foot ulcers among the studied population significantly increases in presence of a history of previous diabetic foot ulceration (2.5% in absence of previous ulceration vs. 44.5% in patients with history of DFU, O.R. 31.76) or diabetes-related lower limb amputation (4% in patients without amputation vs. 51.1% in patients with history of amputation, O.R. 24.94) (p < 0.001). In univariate logistic regression, significant risk factors were:patient’s gender, duration of diabetes, smoking, presence of callus, fissure, joint deformity, limited joint deformity, monofilament insensitivity and abnormal ABI. However, when applying when applying the multivariate regression analysis, diabetes duration, foot fissures, Charcot’s foot, limited joint mobility and both of the peripheral neuropathy and the peripheral vascular insufficiency still retain the significant association with the presence of the diabetic foot disorders as shown in Table 2.
4.
Discussion
The aim of the present work was to determine the prevalence of diabetic foot disorders and the related risk factors among
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Table 2 – A multivariate logistic regression analysis of different risk factors potentially predicting diabetic foot complications. p-Value
Gender (male) DM duration History of smoking Fissure Callus Hallux valgus Hammer toe Flat foot Charcot’s foot Limited joint mobility Monofilament insensitivity ABI ≤ 0.9
0.715 <0.001 0.220 0.018 0.377 0.379 0.113 0.231 <0.001 0.001 <0.001 0.035
patients with diabetes in Egypt. The present study showed high prevalence of diabetic foot disorders among our community. The prevalence of previous foot ulceration was 8.7% (10.3% among males, 7.0% among females). The prevalence of lower limb amputation was 4.4% (6.2% among males, 2.6% among females), while the prevalence of active foot ulceration was 6.1% (8.1% among male population, 4.1% among female population). There is a wide variation reported in the prevalence of diabetic foot ulcers (DFU), ranging between 5.3 and 10.5% [13]. Our study is in agreement with the study conducted by the French Working Group on the Diabetic Foot where 7.2% of the patients had a history of ulceration and/or amputation (6.3% with history of ulceration, 3.24% with history of amputation) and were therefore at very high-risk of (re)ulceration [14]. In agreement with our results, several studies had concluded that foot ulceration is more common in patients with previous history of ulceration or amputation. Apelqvist et al. found a recurrence rate of 34% after 1 year and 70% after 5 years [15]. Murray et al. found a relative risk of 56.8 for an ulcer developing on site of a previous ulceration [16]. Not only that, but also a history of ulceration or amputation is found to be the factor most closely associated with the occurrence of a (new) ulceration [17]. Also it is well known that the probability of a limb amputation on the opposite side following a successful major amputation is 12% in the first year and more than 50% after three years [18]. Patients with foot ulcers may be predisposed to this outcome due to a combination of different pathological factors such as micro- and macro vascular dysfunction, and peripheral nerve damage, creating a very high risk for the patient. In our study the prevalence of diabetic foot disorders was significantly higher among the male population (14.1%) compared to that present among the female population (9.7%). Male gender was identified to be a significant risk factor for the occurrence of diabetic foot disease OR 1.5(95%CI 1.16–2.01). In general, women seem to have fewer complications and a better prognosis than men. The prevalence of peripheral arterial occlusive disease and sensory neuropathy are lower in women with diabetes [19]. Likewise, the prevalence and incidence of amputations and mortality associated with amputations of the foot are significantly lower in women [20]. In women also, foot ulcers and fractures associated with
O.R.
1.078 1.037 1.299 1.719 1.168 1.182 1.360 1.557 3.354 1.748 5.059 1.541
95% C.I. Lower
Upper
0.722 1.019 0.855 1.096 0.828 0.815 0.930 0.755 1.890 1.246 3.661 1.031
1.610 1.055 1.973 2.697 1.649 1.715 1.988 3.214 5.951 2.452 6.993 2.302
Charcot’s arthropathy of the foot have been reported to heal significantly more rapidly than in men [21]. Numerous factors may play a role in the effect of gender on lower extremity morbidity. These may include activity level, smoking behavior, hormonal differences, degree of compliance, level of denial, strength of social support mechanisms, and quality of education as well as the prevalence and severity of vascular disease, neuropathy, and diabetes [22]. In our study, the mean age of the total studied sample was (57.30 ± 10.47). Age as a risk factor was not statistically significant in our study. The reasons for this are unclear but may reflect the fact that older patients in our community are probably less mobile than younger patients, and thus are less exposed to potentially traumatic situations for the ‘at risk’ foot. Elderly patients usually have poor vision, live alone, have other medical problems, and may have lower ability to care for their feet. There was a statistically significant trend between increasing the duration of diabetes and the prevalence of diabetic foot complications as the patient with more than 15 year DM duration showed 6.86 fold increases in the prevalence of DFS compared to patients with less than 5 years DM duration. This is most likely due to other risk factors such as PNP and PAD developing with time [23]. The assessment of dermatological findings revealed that the presence of either fissure or callus was a significant risk factor for the occurrence of diabetic foot disorders. While the presence of toe web maceration and a corn was not significant. This might be attributed to the limitation of cross-sectional studies in identifying the cause and relation of diabetic foot disorders, explaining why our results were not in concordance with published evidence about diabetic foot disorders and toe web maceration. This high prevalence of foot fissures was attributed to dry climate and the tradition of walking barefoot. El-Nahas et al. [24] found that dry skin and calluses were recorded in 44.6% and 5.7%, respectively, while Tinea pedis was found in (43.6%) of the patients. A previous study has suggested that foot sole hardness and foot sole thickness play a role in the development of plantar ulcers [25]. The importance of callus as a precipitating factor for DFU has also been previously confirmed [26]. Also in agreement with our results, Murray et al. stated that the presence of plantar callus, especially in the neuropathic foot, is associated
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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with an increased risk of ulceration. The risk was 77-fold in the cross-sectional part, whereas in the prospective followup, ulceration occurred only at sites of callus, representing an infinite increase in risk [16]. In our study, the prevalence of toe deformities (hallux valgus and hammer toe) was 21.9% and 14.8%, respectively. While the prevalence of limited foot joints mobility (hallux limitus) was 31.4%. Flat foot (pes planus) was present in only 2.8% of our study sample, while Charcot’s foot deformities were present in 3.7%. All these deformities were significantly related to the presence of diabetic foot complications with odds ratio of hallux valgus, hammer toe, hallux limitus, flat foot and Charcot’s foot of 1.51, 2.69, 3.58, 3.1 and 9.96, respectively. In our study, the prevalence of peripheral diabetic neuropathy among the total study population was 29.3%; a prevalence that is higher than a previously reported one from a study done at Mansoura University, where monofilament insensitivity was found in (10.2%) of the patients based on the inability to perceive pressure sensation in 2 or more sites out of 10 sites [24]. Prevalence of DPN in our study is comparable to some other developing countries. An Indian study conducted on 3000 type 2 diabetic patients showed that the prevalence of peripheral neuropathy was as high as 27.5% [27]. Recent studies from Tanzania have also reported a similar prevalence of neuropathy among the diabetic patients (28.1%) [28]. However, some other Arab countries like Sudan [29] and UAE [30] reported a higher prevalence of DPN (37% and 39%, respectively), than that reported in Egypt and other populations [31]. This difference of DPN prevalence may be explained on the basis of ethnicity, different diagnostic testing, and quality of care for of diabetes. Peripheral diabetic neuropathy was found, in our study, to be a highly statistically significant risk factor for the presence of diabetic foot complications. Our study showed that the prevalence of PAD was 11% among the total study population. On the other hand, the Egyptian study from Mansoura University reported a prevalence of only 3.1% among their patients, this difference could be attributed to the different methodology as they relayed only on the absence of any of the foot pulses as a screening tool for lower limb ischemia which might lead to underestimation of the prevalence [24]. According to our results, peripheral vascular disease has been strongly associated with diabetes-related lower extremity complications. In agreement with our results, Boyko et al. reported that whatever the means of measurement, PAD was associated with a three fold increased risk for LEA [32]. In contrast, macrovascular disease, as defined by the ankle-brachial index (<0.80), was not identified as a significant risk factor in either univariate or multivariate models in some other studies [33]. In our study the prevalence of diabetic retinopathy (defined by history of previous laser photocoagulation sessions) was 12.5% among the study population. While the prevalence of diabetic nephropathy was 3.5% among the total study sample. Both microvascular complications of diabetes showed to be significant statistically in association with the presence of diabetic foot complications. In agreement with our results, Boyko et al. in the Seattle Diabetic Foot Study showed that poor vision was independently related to higher ulcer risk. It is possible
that it reflects diabetes severity. Also, poor vision may interfere with the patient’s ability to detect early foot lesions that without attention might progress to non-healing ulcers [23]. Regarding nephropathy, it has been recognized for many years that patients with renal impairment are at increased risk of foot ulceration. In agreement with us, Fernando et al., confirmed that patients at all stages of diabetic nephropathy, even microalbuminuria, have an increased risk of foot ulceration [34]. Indeed, diabetes was shown to be the strongest risk factor for lower extremity amputation in new dialysis patients [35]. An increased risk of DFU with diabetic nephropathy was also detected by The American Diabetes Association Consensus Group [36]. The prevalence of coronary heart diseases was 21.1% among the total study population (29.4% among DFS group vs. 19.9% among control group, O.R. 1.68, p-value = 0.001). The cerebrovascular accidents prevalence was 2.3% among the total study population (4.6% among DFS group vs. 1.9% among control group, O.R. 2.46, p-value = 0.009). Both macrovascular complications showed a statistically significance association with diabetic foot diseases. In agreement with our findings, the Fremantle Diabetes Study showed that CVD (cardiovascular diseases) and PAD are independent predictors of incident LEAs [37]. The risk of a concurrent disease of the coronary vessels in patients suffering from PAD is increased two and a half times compared with patients without disease of the leg vessels [18]. A study performed on an Italian cohort by Pinto et al., showed a worse cerebrovascular risk profile in diabetic patients with diabetic foot than in diabetic subjects without foot ulceration, with a higher prevalence of cardiovascular risk factors and of anamnestic cerebrovascular events and incidence of new cerebrovascular events at a 5-year follow-up [38]. Limitations of our study included: (1) Some limitations were attributed to the cross-section study design. The cross-sectional study design means that our study is a survivor analysis, which again can result in underreporting of DFS. We recommend that a prospective study should be initiated to control for this bias. (2) Further assessment of PAD would be needed like toe pressure assessment or angiography, which was not feasible to be done in a screening clinic.
5.
Conclusion
From the present study one can deduce that a mosaic of risk factors is contributing to the high prevalence of diabetic foot disease in our community. Therefore, screening and detection of early neuropathy, trivial skin lesions should attract health care provider’s attention and empower patients to adhere to their foot care follow-up programs before progression to more serious stages.
Conflict of interest The authors state that they have no conflict of interest.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Acknowledgements “This project is supported by a BRIDGES Grant from the International Diabetes Federation. BRIDGES, an International Diabetes Federation project, is supported by an educational grant from Lilly Diabetes.”
references
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[19] J.C. Alcolado, P.J. Pacy, M. Beevers, et al., Risk factors for peripheral vascular disease in hypertensive subjects with type 2 diabetes mellitus, Diabetes Med 9 (1992) 904–907. [20] D.G. Armstrong, L.A. Lavery, W.H. van Houtum, et al., The impact of gender on amputation, J. Foot Ankle Surg. 36 (1997) 66–69. [21] D.G. Armstrong, L.A. Lavery, T.R. Bushman, Peak foot pressures influence the healing time of diabetic foot ulcers treated with total contact casts, J. Rehabil. Res. Dev. 35 (1998) 1–5. [22] L.A. Lavery, D.G. Armstrong, S.A. Vela, et al., Practical criteria for screening patients at high risk for diabetic foot ulceration, Arch. Intern. Med. 158 (1998) 157–162. [23] Z. Merza, S. Tesfaye, The risk factors for diabetic foot ulceration, Foot 13 (2003) 125–129. [24] M. El-Nahas, H. Gawish, M. Tarshoby, et al., The prevalence of risk factors for foot ulceration in Egyptian diabetic patients, Pract. Diabetes Int. 25 (2008) 362–366. [25] V.J. Thomas, K.M. Patil, S. Radhakrishnan, et al., The role of skin hardness, thickness, and sensory loss on standing foot power in the development of plantar ulcers in patients with diabetes mellitus—a preliminary study, Int. J. Low Extrem. Wounds 2 (2003) 132–139. [26] T. Pavicic, H.C. Korting, Xerosis and callus formation as a key to the diabetic foot syndrome: dermatologic view of the problem and its management, J. Dtsch Dermatol. Ges. 4 (2006) 935–941. [27] A. Ramachandran, C. Snehalatha, K. Satyavani, et al., Prevalence of vascular complications and their risk factors in type 2 diabetes, J. Assoc. Phys. India 47 (1999) 1152–1156. [28] K. Wikblad, B. Smide, A. Bergstrom, et al., Outcome of clinical foot examination in relation to self-perceived health and glycaemic control in a group of urban Tanzanian diabetic patients, Diabetes Res. Clin. Pract. 37 (1997) 185–192. [29] M.N. Elbagir, M.A. Eltom, E.O. Mahadi, et al., Pattern of long-term complications in Sudanese insulin-treated diabetic patients, Diabetes Res. Clin. Pract. 30 (1995) 59–67. [30] F. Al-Maskari, M. El-Sadig, Prevalence of risk factors for diabetic foot complications, BMC Fam. Pract. 8 (2007) 59. [31] A.P. Barbosa, J.L. Medina, E.P. Ramos, et al., Prevalence and risk factors of clinical diabetic polyneuropathy in a Portuguese primary health care population, Diabetes Metab. 27 (2001) 496–502. [32] E.J. Boyko, J.H. Ahroni, D. Davignon, et al., Diagnostic utility of the history and physical examination for peripheral vascular disease among patients with diabetes mellitus, J. Clin. Epidemiol. 50 (1997) 659–668. [33] M.J. McNeely, E.J. Boyko, J.H. Ahroni, et al., The independent contributions of diabetic neuropathy and vasculopathy in foot ulceration. How great are the risks? Diabetes Care 18 (1995) 216–219. [34] D.J. Fernando, A. Hutchison, A. Veves, et al., Risk factors for non-ischaemic foot ulceration in diabetic nephropathy, Diabetes Med. 8 (1991) 223–225. [35] R.A. Speckman, D.L. Frankenfield, S.H. Roman, et al., Diabetes is the strongest risk factor for lower-extremity amputation in new hemodialysis patients, Diabetes Care 27 (2004) 2198–2203. [36] B.E. Sumpio, Foot ulcers, N. Engl. J. Med. 343 (2000) 787–793. [37] W.A. Davis, P.E. Norman, D.G. Bruce, et al., Predictors, consequences and costs of diabetes-related lower extremity amputation complicating type 2 diabetes: the Fremantle Diabetes Study, Diabetologia 49 (2006) 2634–2641. [38] A. Pinto, A. Tuttolomondo, D. Di Raimondo, et al., Cardiovascular risk profile and morbidity in subjects affected by type 2 diabetes mellitus with and without diabetic foot, Metabolism 57 (2008) 676–682.
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Contents lists available at ScienceDirect
Primary Care Diabetes journal homepage: http://www.elsevier.com/locate/pcd
Original research
Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes S.H. Assaad-Khalil a,∗ , A. Zaki b , A. Abdel Rehim a , M.H. Megallaa a , N. Gaber a , H. Gamal a , K.H. Rohoma a a b
Department of Internal Medicine (Unit of Diabetes), Alexandria University, Alexandria, Egypt Department of Biostatistics, Alexandria University, Alexandria, Egypt
a r t i c l e
i n f o
a b s t r a c t
Article history:
Introduction: Multiple pathologies including diabetic neuropathy, peripheral vascular disease
Received 10 June 2012
(PVD) and infection contribute to lower extremities amputation in diabetes.
Received in revised form
Aim: We examined the prevalence of diabetic foot problems and related risk factors in Egypt.
30 August 2014
Subjects and methods: Between July 2008 and December 2009, 1000 male and 1000
Accepted 31 October 2014
female consecutive adult patients with diabetes (≥18-year-old) attending the Alexan-
Available online xxx
dria University Diabetic Foot Screening Clinic were surveyed for history/presence of foot ulcers and/or amputations, skin/nail changes, joint mobility, sensory neuropathy (10 g-
Keywords:
Semmes–Weinstein Monofilament) and peripheral vascular disease (PVD) using Ankle
Risk factors
Brachial Index (ABI).
Prevalence
Results: The majority of patients had type 2 diabetes (96.75%) with a mean age of 57.30 ± 10.47
Diabetic foot
years and a mean disease duration of 11.76 ± 8.26 years. The mean body mass index was
Egypt
32.84 ± 6.31 kg/m2 with 29.55% being current or ex-smokers. In these subjects, 4.4% had a past history of non-traumatic amputation (male:female: 6.2% vs. 2.6%, p < 0.001); 6.1% had past history (10.3% vs. 7%, p = 0.009) and 8.7% had active foot ulceration (8.1% vs. 4.1% p < 0.001) with a male preponderance. The prevalence of sensory neuropathy was 29.3% (M:F: 30.7%: 27.9%) and peripheral vascular disease (PVD) was 11% (M:F 11.8%:10.2%). Diabetic foot complications were associated with disease duration (p < 0.001), history of coronary artery disease (p = 0.001), stroke (p = 0.009), PVD (p < 0.001), laser photocoagulation (p < 0.001), sensory neuropathy (p < 0.001) and renal replacement therapy (p < 0.001). On multivariate analysis, diabetes duration, foot fissures, Charcot’s foot, limited joint mobility, PVD and sensory neuropathy remained independently associated with diabetic foot disorders. Conclusion: In Egypt, a mosaic of risk factors contributes to the high prevalence of diabetic foot disease in type 2 diabetes. These findings call for regular assessment of vascular, neuropathic and skin status to prevent these serious foot complications. © 2014 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.
∗
Corresponding author. Tel.: +20 1222197789; fax: +20 34833321. E-mail address: [email protected] (S.H. Assaad-Khalil).
http://dx.doi.org/10.1016/j.pcd.2014.10.010 1751-9918/© 2014 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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1.
Introduction
The diabetic foot syndrome encompasses a number of pathologies, including diabetic neuropathy, peripheral vascular disease, Charcot’s neuroarthropathy, foot ulceration, osteomyelitis, and the potentially preventable end point, amputation [1]. Subjects with diabetic foot problems are also likely to harbor other associated complications of diabetes such as nephropathy, retinopathy, ischemic heart disease and cerebrovascular disease [2]. The burden of diabetic foot disease is set to increase in the future since the contributory factors to foot disease, such as peripheral neuropathy and vascular disease, are present in more than 10% of people at the time of diagnosis of type 2 diabetes [3]. The annual populationbased incidence of foot ulceration is approximately 1–4% [4], and the prevalence ranges from 4% to 10% which suggests that lifetime risk can range from 15% to as high as 25% [5]. Diabetic foot ulcers/infections negatively impact quality of life (QOL), increase morbidity and mortality and also incur a substantial economic burden for society, patients and their families [6]. Amputation is a serious consequence of diabetes. Lower limb amputation is performed 10–30 times more frequently among diabetic than among general population [7]. Every 30 s, somewhere in the world, a lower limb is lost as a complication of diabetes [8]. One report noted that more than 80% of non-traumatic lower extremity amputations (LEAs) are performed in diabetic patients [9]. and more than 85% of these were precipitated by a foot ulcer that subsequently progressed to a severe infection [7]. Individuals are at high risk for amputation of the contralateral limb if they have already undergone amputation of one limb. Furthermore, 30–50% of first-episode amputations will progress to subsequent amputations within 1–3 years. Amputation carries with it a significantly elevated mortality at follow-up, ranging from 13% to 40% at 1 year to 39–80% at 5 years [10]. The study of the epidemiology of diabetic foot disease has been beset by numerous problems related to diagnostic tests and population selection. Few studies have reported the prevalence of diabetic foot disorders in Egypt. The aim of this work was to detect the prevalence of diabetic foot problems among Egyptian population, related risk factors and the associated diabetes complications among patients with ulceration or amputation.
2.
Methods
2.1.
Research design
This is a cross sectional study to estimate the prevalence of diabetic foot complications among attendants of the Diabetic Foot Screening Clinic (DFSC) in Alexandria. A nested case control study was undertaken to assess risk factors for the development of diabetic foot complications.
2.2.
Setting and study population
Alexandria Main University Hospital runs two diabetes clinics, a general diabetes clinic and a Diabetic Foot Screening Clinic (DFSC). The later was recently established by a fund from the IDF BRIDGES to be a screening and a preventive center in addition to provision of primary foot care services like callus debridement, nail cutting, treatment of foot infections etc. All patients attending the general diabetes clinic (whether from Alexandria or the surrounding governorates) were given appointments to attend the diabetic foot clinic (without prior selection). Response rate was high (93.4%) as we were the only provider of foot care service in that region of the country, so the attendance rate was 4–6 patients per day amounting to around one thousand patients per year. Enrolment in the diabetic foot registry was done based on the order of patient attendance. Professors, consultants, specialist, residents, and house officers, together with trained nurses and health workers participated in the clinic.
2.3.
Sample size
According to previous studies we expect the average prevalence of diabetic foot complications to be around 6% in adult males and females. To achieve a study power equal to 80%, at confidence level 95%, and with precision ±2 around our estimate, the calculated sample size was found to be equal to 958. Accordingly, we planned to recruit 1000 male and 1000 female consecutive diabetic patients from among attendants of the DFSC for routine check up during the period from July 2008 to December 2009. Only Patients aged above 18 years old who had been already diagnosed with diabetes according to WHO criteria were eligible.
2.4.
Data collection
Study participants had a face-to-face interview with one the physicians to collect data using a standardized questionnaire [11] about the following variables: Demographic characteristics, duration of DM, symptoms of neuropathy using the diabetic neuropathy symptom (DNS) score [12], smoking habits, past history of related co morbidities like hypertension, coronary heart diseases, cerebrovascular stroke, claudication, revascularization, renal transplantation or dialysis and laser photocoagulation. All participants were clinically examined. The general clinical examination was carried by physicians (consultant, specialist, or resident) and included measurement of blood pressure, recording of the patient weight and height with calculation of body mass index (BMI). The feet were thoroughly examined for the presence of foot ulcers and/or amputations. Foot deformities including halux valgus, hammer/claw toe, flat foot and Charcot’s foot. The skin of the foot was also assessed for presence of callus, corns, fissuring and presence of toe web macerations. The foot nails were examined to detect presence of nail dystrophies, ingrowing nails & onychomychosis. Foot joint mobility was assessed to detect limited joint mobility which was defined as less than 50◦ of non-weight bearing passive dorsiflexion of the hallux.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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The neurological status of the foot was assessed using 10 g-Semmes–Weinstein Monofilament examination. A 5.07 Semmes–Weinstein nylon monofilament was employed to apply a consistent 10 g force on 9 different sites; planter surface of the first, third and fifth toes; under head of first, third and fifth metatarsal bones; planter surface of the mid-foot; heel and dorsal space between the first and second toe. The sensation of pressure using the buckling 10-g monofilament was first demonstrated to the patient on a proximal site. Then with the patients unable to see their feet, the monofilament was placed on the plantar surface of the foot at right angles to the skin and the pressure increased until the filament buckled. The patients were asked to say “yes” when they felt something. Areas of callus were avoided. A foot is classified to have loss of protective sensation or sensory neuropathy when less than seven sites were felt by the patient. A foot is classified as normal if seven or more sites were felt by the patient. Peripheral vascular status of the foot was assessed by measuring Ankle Brachial Index (ABI) for dorsalis pedis & posterior tibial arteries of both feet. Ankle pressures were measured using a standardized Doppler ultrasonic device (5 MHz; Nicolet Elite 200 R, VIASYS Healthcare Inc., Madison, WI, USA). ABI was calculated as the ratio of the higher of the two systolic pressures (from posterior tibial and dorsalis pedis) at the ankle to the higher reading of the right and left brachial artery pressures. Pressures in each leg were measured and ABI was calculated separately for each leg. In the case of a missing ABI value in one leg, the value from the other was used, and likewise for missing brachial artery pressure values in one arm. Peripheral arterial disease (PAD) was defined as an ABI of ≤0.9 in at least one leg. The lower ABI between the two legs was used to define PAD. The patient was considered to have diabetic foot disorder if he has any of the following disorders attributed to his diabetic condition: amputation, active foot ulcer or previous foot ulcer. Individuals with foot disorders were assigned to only one of the mutually exclusive groups. The diabetic patient with amputation was assigned only to the amputation group whether or not he had active ulcer or history of previous ulcer. An individual with diabetic active foot ulcer and not having amputation was assigned only as having active foot ulcer whether or not he had history of previous ulcer. The patients assigned to the group with previous ulcer, gave this history but did not suffer amputation or current active foot ulcer.
2.5.
3
Association between co morbidities, skeletal deformities and foot joints mobility and the development of diabetic foot disorders was tested using Chi square test. All risk factors significantly associated with diabetic foot complications (p < 0.05) in the bivariate analysis were included as independent variables in a multivariate logistic model with diabetic foot complication as an outcome variable. The adjusted OR with 95%CI for each risk factor was calculated controlling for the effect of other co variables.
3.
Results
The study sample included 1000 males and 1000 females, the majority were type 2 diabetes (96.75%). The mean age was 57.30 ± 10.47 years and the mean known duration of diabetes was 11.76 ± 8.26 years. The mean BMI of our patients was 32.84 ± 6.31 kg/m2 . The habit of smoking (current/ex-smoker) was present in 29.55% of the total population. The prevalence of non-traumatic amputation was 4.4% (6.2% among males and 2.6% among females),with statistical significance (p < 0.001). Active foot ulceration was identified in 6.1% (8.1% among males, 4.1% among females),with statistical significance (p < 0.001). While the prevalence of past foot ulceration was 8.7%(10.3% among males and 7% among females, with statistical significance (p = 0.009). Therefore the overall prevalence of ulceration and amputation was 11.85%. The overall prevalence among males was higher than that among females (14.1% and 9.7%, respectively) with a significant relationship (p = 0.002). Diabetic foot disorders, was defined by the presence of non-traumatic foot amputation or current active foot ulcer or history of previous foot ulcer. There was a statistically significant trend for the increase in the prevalence of diabetic foot disorders with the increase of the duration of DM among our study population (p < 0.001) as shown in Fig. 1. There was a significant association between the prevalence of diabetic foot disorders (DFD) and both macrovascular and microvascular complications (Table 1). There was a statistically significant relationship between the presence of several dermatological examination findings and the prevalence of diabetic foot disorders. These findings include foot fissures (17.53% in patients with fissures vs. 11.3% in patients did not have fissures, p = 0.011), foot callus (14.76%
Ethical submission
The study was reviewed and approved by the Institutional Review Board/Research Ethics Committee of the Faculty of Medicine, Alexandria University, Alexandria; Egypt.
2.6.
Statistical analysis
Statistical analysis was performed using SPSS version 18.0 (SPSS Inc, Chicago, Illinois, USA). Quantitative variables like age, BMI and duration of diabetes were presented as mean ± SD, while qualitative variables like sex, smoking (current/ex-smoker/non smokers), frequency of different diabetic foot disorder were presented as percentage.
Fig. 1 – Prevalence of diabetic foot complications in the study population presented according to the duration of diabetes.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Table 1 – Association between co morbidities and diabetic foot disorders in 2000 diabetic patients. Comorbiditiy
Hypertension
Coronary artery disease
Cerebrovascular stroke
Claudication
Revascularization
Free f
Yes (N = 1024) No (N = 976)
819
Yes (N = 421) No (N = 1579)
310
Yes (N = 45) No (N = 1955) Yes (N = 213) No (N = 1787) Yes (N = 25) No (N = 1975)
Renal transplantation or dialysis.
Yes (N = 69) No (N = 1931)
Laser photocoagulation
Yes (N = 250) No (N = 1750)
∗
798
1307
32 1585
159 1458
7 1610
69 136
136 1481
p-Value*
Diabetic foot disorders History of foot ulcer n = 173
Active foot ulcer n = 122
Amputation n = 88
92 8.98% 81 8.30%
56 5.47% 66 6.76%
57 5.57% 31 3.18%
0.198
52 12.35% 121 7.66%
33 7.84% 89 5.64%
26 6.16% 62 3.93%
0.001*
7 15.56% 166 8.49%
5 11.11% 117 5.98%
1 2.22% 87 4.45%
0.009*
27 12.68% 146 8.17%
13 6.10% 109 6.10%
14 6.57% 74 4.14%
0.005*
7 28% 166 8.41%
6 24% 116 5.87%
5 20% 83 4.20%
<0.001*
11 15.94% 162 8.39%
7 10.14 115 5.96%
6 8.70% 82 4.25%
0.001*
51 20.4% 122 6.97%
33 13.2% 89 5.09%
30 12% 58 3.31%
<0.001*
indicates a statistically significant difference.
in patient with vs. 10.92% in patient without callus, p = 0.021). On the other hand, the presence of corns or toe web maceration did not show significant relation with the prevalence of diabetic foot disorders. In our study, the prevalence of peripheral diabetic neuropathy among the total study population was 29.3%. (30.7% in males and 27.9% in females with statistical significance; p = 0.168). The presence of diabetic peripheral neuropathy was defined based on the inability to perceive 2 or more sites out of 9 when using the 10 g Semmes–Weinstein monofilament. Peripheral diabetic neuropathy was found to be a highly statistically significant risk factor for the presence of diabetic foot complications. The prevalence of PAD was (11%) among the total study population. The prevalence was (11.8%) among males and (10.2%) among females. PAD was defined based on the assessment of Ankle–Brachial Index (ABI) <0.9. Presence of PAD showed a high statistical significance with the occurrence of diabetic foot amputation and ulceration (27.9% in patients with ulceration and amputation vs. 11.9% diabetics without ulceration and amputations, O.R. = 2.65) (p < 0.001).
The prevalence of active foot ulcers among the studied population significantly increases in presence of a history of previous diabetic foot ulceration (2.5% in absence of previous ulceration vs. 44.5% in patients with history of DFU, O.R. 31.76) or diabetes-related lower limb amputation (4% in patients without amputation vs. 51.1% in patients with history of amputation, O.R. 24.94) (p < 0.001). In univariate logistic regression, significant risk factors were:patient’s gender, duration of diabetes, smoking, presence of callus, fissure, joint deformity, limited joint deformity, monofilament insensitivity and abnormal ABI. However, when applying when applying the multivariate regression analysis, diabetes duration, foot fissures, Charcot’s foot, limited joint mobility and both of the peripheral neuropathy and the peripheral vascular insufficiency still retain the significant association with the presence of the diabetic foot disorders as shown in Table 2.
4.
Discussion
The aim of the present work was to determine the prevalence of diabetic foot disorders and the related risk factors among
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Table 2 – A multivariate logistic regression analysis of different risk factors potentially predicting diabetic foot complications. p-Value
Gender (male) DM duration History of smoking Fissure Callus Hallux valgus Hammer toe Flat foot Charcot’s foot Limited joint mobility Monofilament insensitivity ABI ≤ 0.9
0.715 <0.001 0.220 0.018 0.377 0.379 0.113 0.231 <0.001 0.001 <0.001 0.035
patients with diabetes in Egypt. The present study showed high prevalence of diabetic foot disorders among our community. The prevalence of previous foot ulceration was 8.7% (10.3% among males, 7.0% among females). The prevalence of lower limb amputation was 4.4% (6.2% among males, 2.6% among females), while the prevalence of active foot ulceration was 6.1% (8.1% among male population, 4.1% among female population). There is a wide variation reported in the prevalence of diabetic foot ulcers (DFU), ranging between 5.3 and 10.5% [13]. Our study is in agreement with the study conducted by the French Working Group on the Diabetic Foot where 7.2% of the patients had a history of ulceration and/or amputation (6.3% with history of ulceration, 3.24% with history of amputation) and were therefore at very high-risk of (re)ulceration [14]. In agreement with our results, several studies had concluded that foot ulceration is more common in patients with previous history of ulceration or amputation. Apelqvist et al. found a recurrence rate of 34% after 1 year and 70% after 5 years [15]. Murray et al. found a relative risk of 56.8 for an ulcer developing on site of a previous ulceration [16]. Not only that, but also a history of ulceration or amputation is found to be the factor most closely associated with the occurrence of a (new) ulceration [17]. Also it is well known that the probability of a limb amputation on the opposite side following a successful major amputation is 12% in the first year and more than 50% after three years [18]. Patients with foot ulcers may be predisposed to this outcome due to a combination of different pathological factors such as micro- and macro vascular dysfunction, and peripheral nerve damage, creating a very high risk for the patient. In our study the prevalence of diabetic foot disorders was significantly higher among the male population (14.1%) compared to that present among the female population (9.7%). Male gender was identified to be a significant risk factor for the occurrence of diabetic foot disease OR 1.5(95%CI 1.16–2.01). In general, women seem to have fewer complications and a better prognosis than men. The prevalence of peripheral arterial occlusive disease and sensory neuropathy are lower in women with diabetes [19]. Likewise, the prevalence and incidence of amputations and mortality associated with amputations of the foot are significantly lower in women [20]. In women also, foot ulcers and fractures associated with
O.R.
1.078 1.037 1.299 1.719 1.168 1.182 1.360 1.557 3.354 1.748 5.059 1.541
95% C.I. Lower
Upper
0.722 1.019 0.855 1.096 0.828 0.815 0.930 0.755 1.890 1.246 3.661 1.031
1.610 1.055 1.973 2.697 1.649 1.715 1.988 3.214 5.951 2.452 6.993 2.302
Charcot’s arthropathy of the foot have been reported to heal significantly more rapidly than in men [21]. Numerous factors may play a role in the effect of gender on lower extremity morbidity. These may include activity level, smoking behavior, hormonal differences, degree of compliance, level of denial, strength of social support mechanisms, and quality of education as well as the prevalence and severity of vascular disease, neuropathy, and diabetes [22]. In our study, the mean age of the total studied sample was (57.30 ± 10.47). Age as a risk factor was not statistically significant in our study. The reasons for this are unclear but may reflect the fact that older patients in our community are probably less mobile than younger patients, and thus are less exposed to potentially traumatic situations for the ‘at risk’ foot. Elderly patients usually have poor vision, live alone, have other medical problems, and may have lower ability to care for their feet. There was a statistically significant trend between increasing the duration of diabetes and the prevalence of diabetic foot complications as the patient with more than 15 year DM duration showed 6.86 fold increases in the prevalence of DFS compared to patients with less than 5 years DM duration. This is most likely due to other risk factors such as PNP and PAD developing with time [23]. The assessment of dermatological findings revealed that the presence of either fissure or callus was a significant risk factor for the occurrence of diabetic foot disorders. While the presence of toe web maceration and a corn was not significant. This might be attributed to the limitation of cross-sectional studies in identifying the cause and relation of diabetic foot disorders, explaining why our results were not in concordance with published evidence about diabetic foot disorders and toe web maceration. This high prevalence of foot fissures was attributed to dry climate and the tradition of walking barefoot. El-Nahas et al. [24] found that dry skin and calluses were recorded in 44.6% and 5.7%, respectively, while Tinea pedis was found in (43.6%) of the patients. A previous study has suggested that foot sole hardness and foot sole thickness play a role in the development of plantar ulcers [25]. The importance of callus as a precipitating factor for DFU has also been previously confirmed [26]. Also in agreement with our results, Murray et al. stated that the presence of plantar callus, especially in the neuropathic foot, is associated
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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with an increased risk of ulceration. The risk was 77-fold in the cross-sectional part, whereas in the prospective followup, ulceration occurred only at sites of callus, representing an infinite increase in risk [16]. In our study, the prevalence of toe deformities (hallux valgus and hammer toe) was 21.9% and 14.8%, respectively. While the prevalence of limited foot joints mobility (hallux limitus) was 31.4%. Flat foot (pes planus) was present in only 2.8% of our study sample, while Charcot’s foot deformities were present in 3.7%. All these deformities were significantly related to the presence of diabetic foot complications with odds ratio of hallux valgus, hammer toe, hallux limitus, flat foot and Charcot’s foot of 1.51, 2.69, 3.58, 3.1 and 9.96, respectively. In our study, the prevalence of peripheral diabetic neuropathy among the total study population was 29.3%; a prevalence that is higher than a previously reported one from a study done at Mansoura University, where monofilament insensitivity was found in (10.2%) of the patients based on the inability to perceive pressure sensation in 2 or more sites out of 10 sites [24]. Prevalence of DPN in our study is comparable to some other developing countries. An Indian study conducted on 3000 type 2 diabetic patients showed that the prevalence of peripheral neuropathy was as high as 27.5% [27]. Recent studies from Tanzania have also reported a similar prevalence of neuropathy among the diabetic patients (28.1%) [28]. However, some other Arab countries like Sudan [29] and UAE [30] reported a higher prevalence of DPN (37% and 39%, respectively), than that reported in Egypt and other populations [31]. This difference of DPN prevalence may be explained on the basis of ethnicity, different diagnostic testing, and quality of care for of diabetes. Peripheral diabetic neuropathy was found, in our study, to be a highly statistically significant risk factor for the presence of diabetic foot complications. Our study showed that the prevalence of PAD was 11% among the total study population. On the other hand, the Egyptian study from Mansoura University reported a prevalence of only 3.1% among their patients, this difference could be attributed to the different methodology as they relayed only on the absence of any of the foot pulses as a screening tool for lower limb ischemia which might lead to underestimation of the prevalence [24]. According to our results, peripheral vascular disease has been strongly associated with diabetes-related lower extremity complications. In agreement with our results, Boyko et al. reported that whatever the means of measurement, PAD was associated with a three fold increased risk for LEA [32]. In contrast, macrovascular disease, as defined by the ankle-brachial index (<0.80), was not identified as a significant risk factor in either univariate or multivariate models in some other studies [33]. In our study the prevalence of diabetic retinopathy (defined by history of previous laser photocoagulation sessions) was 12.5% among the study population. While the prevalence of diabetic nephropathy was 3.5% among the total study sample. Both microvascular complications of diabetes showed to be significant statistically in association with the presence of diabetic foot complications. In agreement with our results, Boyko et al. in the Seattle Diabetic Foot Study showed that poor vision was independently related to higher ulcer risk. It is possible
that it reflects diabetes severity. Also, poor vision may interfere with the patient’s ability to detect early foot lesions that without attention might progress to non-healing ulcers [23]. Regarding nephropathy, it has been recognized for many years that patients with renal impairment are at increased risk of foot ulceration. In agreement with us, Fernando et al., confirmed that patients at all stages of diabetic nephropathy, even microalbuminuria, have an increased risk of foot ulceration [34]. Indeed, diabetes was shown to be the strongest risk factor for lower extremity amputation in new dialysis patients [35]. An increased risk of DFU with diabetic nephropathy was also detected by The American Diabetes Association Consensus Group [36]. The prevalence of coronary heart diseases was 21.1% among the total study population (29.4% among DFS group vs. 19.9% among control group, O.R. 1.68, p-value = 0.001). The cerebrovascular accidents prevalence was 2.3% among the total study population (4.6% among DFS group vs. 1.9% among control group, O.R. 2.46, p-value = 0.009). Both macrovascular complications showed a statistically significance association with diabetic foot diseases. In agreement with our findings, the Fremantle Diabetes Study showed that CVD (cardiovascular diseases) and PAD are independent predictors of incident LEAs [37]. The risk of a concurrent disease of the coronary vessels in patients suffering from PAD is increased two and a half times compared with patients without disease of the leg vessels [18]. A study performed on an Italian cohort by Pinto et al., showed a worse cerebrovascular risk profile in diabetic patients with diabetic foot than in diabetic subjects without foot ulceration, with a higher prevalence of cardiovascular risk factors and of anamnestic cerebrovascular events and incidence of new cerebrovascular events at a 5-year follow-up [38]. Limitations of our study included: (1) Some limitations were attributed to the cross-section study design. The cross-sectional study design means that our study is a survivor analysis, which again can result in underreporting of DFS. We recommend that a prospective study should be initiated to control for this bias. (2) Further assessment of PAD would be needed like toe pressure assessment or angiography, which was not feasible to be done in a screening clinic.
5.
Conclusion
From the present study one can deduce that a mosaic of risk factors is contributing to the high prevalence of diabetic foot disease in our community. Therefore, screening and detection of early neuropathy, trivial skin lesions should attract health care provider’s attention and empower patients to adhere to their foot care follow-up programs before progression to more serious stages.
Conflict of interest The authors state that they have no conflict of interest.
Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010
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Acknowledgements “This project is supported by a BRIDGES Grant from the International Diabetes Federation. BRIDGES, an International Diabetes Federation project, is supported by an educational grant from Lilly Diabetes.”
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Please cite this article in press as: S.H. Assaad-Khalil, et al., Prevalence of diabetic foot disorders and related risk factors among Egyptian subjects with diabetes, Prim. Care Diab. (2014), http://dx.doi.org/10.1016/j.pcd.2014.10.010