p r i m a r y c a r e d i a b e t e s 3 ( 2 0 0 9 ) 219–224

Contents lists available at ScienceDirect

Primary Care Diabetes

journal homepage: http://www.elsevier.com/locate/pcd

Original research

Assessment of risk factors in diabetic foot ulceration

and their impact on the outcome of the disease

Emad Naeem Hokkam ∗

Department of surgery, Faculty of Medicine, Suez Canal University, Ismailia, Egypt

a r t i c l e i n f o a b s t r a c t

Article history: Aims: The current study aims to identify risk factors for diabetic foot ulcer and their impact
Received 25 April 2009 on the outcome of the disease.
Received in revised form Methods: Three hundred diabetic patients were enrolled in the study. One hundred eighty
7 August 2009 subjects with diabetic foot ulcer and 120 diabetic controls without foot lesions. All expected
Accepted 14 August 2009 risk factors were studied in all patients and after a follow up period, patients with diabetic
Available online 23 September 2009 foot ulcer were classified into group A (patients with healed ulcers) and group B (patients
with persistent ulcer or ended by amputation). The risk factors were reanalyzed in both
Keywords: groups to find out their impact on the outcome of the disease.
Diabetes mellitus Results: The following variables were significant factors for foot ulceration: Male gender
Foot ulcer (P = 0.009), previous foot ulcer (P = 0.003), peripheral vascular disease (P = 0.004), and periph-
Risk factors eral neuropathy (P = 0.006). Also lack of frequent foot self-examination was independently
related to foot ulcer risk. The outcome was related to longer diabetes duration (P = 0.004),
poor glycaemic control (P = 0.006) and anaemia (P = 0.003) and presence of infection (P < 0.001).
Conclusions: Peripheral vascular disease and peripheral neuropathy together with lack of foot
self-examination, poor glycaemic control and anaemia are main significant risk factors for
diabetic foot ulceration.
© 2009 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.

wide, its incidence is approaching the epidemic proportions

1. Introduction
Diabetes mellitus is a major cause of morbidity and mortality;
it is often referred to as a silent killer because it annu-
ally contributes to approximately 18% of all deaths among
patients who are age 25 and older. The prevalence of dia-
betes mellitus worldwide has increased dramatically during
the past few decades, and it is expected to increase even
more in the future [1–3]. It is now considered the fourth or
fifth leading cause of death in most developed countries, with
about 194 million people suffering from the disease world-
[4].
Further, the prevalence of disease complications is two to
four times higher among adults with diabetes than among
adults without it [2]. These complications can be prevented
or delayed with optimal health care and improved preventive
care practices [2,5]. However, the clinical care received by many
persons with diabetes and their preventive care practices are
suboptimal [6,7].
Foot ulceration is one of the most serious and costly com-
plications of diabetes worldwide. The prevalence of diabetic
foot ulcers has been estimated to be 3–8% [8]. Further, the life-

∗
Tel.: +20 161200090; fax: +20 643208543.
E-mail address: ehokkam@gmail.com.
1751-9918/$ – see front matter © 2009 Primary Care Diabetes Europe. Published by Elsevier Ltd. All rights reserved.
doi:10.1016/j.pcd.2009.08.009
220 p r i m a r y c a r e d i a b e t e s 3 ( 2 0 0 9 ) 219–224
time risk of a person with diabetes for developing a foot ulcer
is estimated at 15–25% [9–11]. In recent years, major progress
has been in the recognition of the problem and in the under-
standing and management of the disease. Foot ulcerations
usually result from the interpretations of many factors includ-
ing neuropathy, bone affection and peripheral angiopathy [12].
The prevention of foot disease relies on the identification of
high-risk patients and avoidance of triggering events, such as
ill-fitting shoes, smoking, walking barefoot or poor self-care
[13].
The worst and most feared outcome of diabetic foot ulcers
is lower limb amputation [14]. Diabetes continues to be the
leading cause of lower limb amputation worldwide. The WHO
has estimated that there is approximately 250,000 lower limb
amputation per year in diabetic patients in Europe alone [15].
A foot ulcer precedes and is responsible for 85% of these
amputations [16–18]. 15–27% of all foot ulcers result in sur-
gical removal of bone. In addition to radically affecting the
quality of life of the patient; this represents a major problem
economically for health care systems [19–23].
Several studies suggest that amputations can be reduced
by 40–85% when high-risk patients are identified and pro-
vided with a multispecialty treatment approach that focuses
on preventive strategies [24,25]. So, identification of patients
at risk of foot ulceration is of paramount importance. Many
efforts have been initiated to find out these factors which are
implicated in the development and persistence of diabetic foot
ulcer. Avoidance of these risk factors will help in establish-
ment of efficacious treatments and preventive care measures.
It is therefore of interest to investigate these factors and their
impact on the disease [26].
2. Methods
The study was carried out at the surgery clinic of the Suez
Canal University Hospital, Ismailia, Egypt. Over a 18 month
period (between August 2007 and January 2009), 300 consecu-
tively attending diabetic patients were prospectively recruited.
One hundred eighty subjects with diabetic foot ulcer and 120
diabetic controls without foot ulcers. Cases were defined as
subjects that were admitted to hospital for diabetic foot ulcer
while controls were patients from the same outpatient pop-
ulation that are diabetic but had no foot ulcer. They were
admitted for another medical or surgical reason mentioned
on their admission records.
All patients received a medical interview and a physical
examination. Data recorded included age, gender, diabetes
duration, type of diabetes and type of treatment. Information
about chronic medical illness and frequent foot examination
was obtained. Patients were considered to have chronic med-
ical illness if they had medical impairment that necessitating
acute hospitalization exceeding 30 days, or medical supervi-
sion and rehabilitation of 3 months or longer in another care
setting [27], while they were considered to follow frequent
foot examination if they used to examine and clean their feet
regularly and sought medical advice when needed. Also, all
patients were asked if they had history of smoking, previous
foot ulcers or previous amputation. The socioeconomic status
was classified into low and accepted according to the monthly
Fig. 1 – infected diabetic foot ulcer.
income of each person (low ≤150 L.E & accepted >150 L.E) men-
tioned in the Egypt human development report 2008 prepared
by United Nations Development Programme [28].
A standard general health examination was performed to
all patients focusing on measurement of height and weight
(without shoes) for calculation of body mass index (BMI). We
calculated BMI as weight in kilograms divided by the square
of height in meters. Patients were classified as underweight
(BMI < 18.5 kg/m2 ), of normal weight (BMI 18.5 to <25 kg/m2 ),
overweight (BMI 25 to <30 kg/m2 ), and obese (BMI ≥ 30 kg/m2 )
[29]. Locally, meticulous examination of the feet was done for
every patient. The presence of infection, peripheral sensory
neuropathy and peripheral vascular disease were the three
main items looked for during the local examination. Also the
feet of the controls were examined for the presence of any
ulceration, gangrene or infections. Any patient with any form
of foot pathology was excluded from the control group.
In the foot diseased subjects, determination of infection
was made clinically by looking for the classical signs of inflam-
mation, rubor, calor, dolor, tumor and local signs of infection,
such as (sero) purulent exudate, foul smell, and gangrene, and
more systemic signs such as fever, chills, and general malaise
(Fig. 1).
Sensory neuropathy was considered positive if three or
more sensory modalities were absent [30,31]. The main exam-
ined sensory modalities were pain, touch and vibration sense
over the medial malleollus of the affected foot. The patient
was considered to have peripheral vascular disease that may
affect the development of ulcer if there was absent pulsa-
tion of either the dorsalis pedis or posterior tibial artery, or
ankle–brachial systolic blood pressure index <0.80 [32].
Chronic renal insufficiency was stratified as creatinine
>4.0 mg/dl, current dialysis or a history of renal transplan-
tation [33] while the presence of diabetic retinopathy was
assessed by one independent ophthalmologist. It was con-
sidered positive when simple or proliferative changes were
observed at fundus examination [34]. Laboratory investiga-
tions included blood glucose level, haemoglobin level and lipid
profile for each patient.
Patients with diabetic foot ulceration were followed up to a
maximum period of 6 months. At the end of the study period,
 p r i m a r y c a r e d i a b e t e s 3 ( 2 0 0 9 ) 219–224 221

those patients were classified into two groups according to
the outcome of the disease. One group was representing the
patients with healed ulcers and the other group who’s ulcer
not healed or ended by amputation of the affected limb. Again,
the previously mentioned risk factors were studied in both
groups to find out their impact on the outcome of the disease.
Data analyses were performed using the SPSS 11.5 software
statistical package. Statistical significance was determined by
the chi-square test for categorical data.
3. Results
Males were significantly commoner in foot diseased group
(P = 0.009). They represented 65% of the group while both sexes
were almost equal in control group. Although subjects were
older compared to controls (58.3 ± 12.9 vs 56.5 ± 13.8), the age
difference was not significant (P > 0.05). The average duration
was not statistically significant (P > 0.05).
Most of the patients in foot diseased group were of type
II diabetes mellitus (170 cases) and represent 94% while the
others are of type I (6%). The same was recorded in controls
but in a lesser degree where type II diabetes mellitus repre-
sent 80%. The type of treatment was not significant between
subjects and controls (P > 0.05). Patients in foot diseased group
were more likely to have past history of diabetic foot ulcers
(66%).
Among the significant factors for diabetic foot ulceration
were medical co-morbidity and lack of frequent foot self-
examination. One hundred and eight patients (60%) with foot
ulcer had chronic medical illness beside the diabetes. The
most common of these are the hypertension, chronic heart
diseases and obesity (32%, 17% and 11% respectively). Only
14 patients (8%) with foot ulcer experienced frequent foot
examination by themselves. They used to examine and clean
their feet regularly and sought medical advice when needed.
Smoking was recorded in 25% and 21% of subjects and con-
trols respectively. It was not statistically significant (P > 0.05).
Although patients who are living in rural areas and those with
low socioeconomic status and lower educational levels repre-
sent the majority of the studied patients, this phenomenon is
more marked in foot diseased group (85%).
Sensory neuropathy was found in 62% of subjects and
38% of controls, whereas 69% of subjects and 35% of controls
had a peripheral arterial disease. Both neuropathy and vascu-
lar insufficiency were significant risk factors for diabetic foot
ulceration (P = 0.006 and 0.004 respectively). A positive relation
was present between the probability of having diabetic foot
ulcer and poor glycaemic control and anaemia (P = 0.005 and
0.004 respectively). On the other hand, dyslipidaemia, chronic
renal insufficiency, retinopathy and body weight were not sig-
nificant factors (P > 0.05). Table 1 shows the main risk factors
for diabetic foot ulcer among subjects and controls.
Fortunately, there was no drop out in the foot diseased
group and each patient could be followed up for a maximum
period of 6 months. They were classified into group A (patients
with healed ulcers) and group B (patients with persistent ulcer
or ended by amputation). Group A was 111 patients (62%) while
group B was 69 patients (38%).
Both groups were comparable regarding age, sex, type of
diabetes, smoking and previous history of foot ulceration.
The outcome was not affected significantly by the presence
of nephropathy or retinopathy (P > 0.05). In group B, diabetes
duration was longer (16 ± 10 vs 9 ± 7 years) and insulin treat-
ment was more common (84% vs 30%). Blood glucose level was
significantly higher in group B while haemoglobin level was
significantly higher in group A (P = 0.006, P = 0.003 respectively).
The signs of sensory neuropathy and medical co-morbidities
were frequent in both groups without statistical difference.
The development of diabetic foot ulcer was strongly related
to the presence of infection, absent palpable pedal pulses and
lack of foot self-examination (P < 0.001, 0.004 and 0.002 respec-
tively). Table 2 summarizes the main differences between
group A and group B.
4. Discussion
The development of a foot ulcer has traditionally been con-
sidered to result from a combination of peripheral vascular

Table 1 – The main risk factors for diabetic foot ulcer.

Foot diseased group Control group P value

(n = 180) (n = 120)
Age 58.3 ± 12.9 56.5 ± 13.8 >0.05
Duration of diabetes 17.7 ± 11.8 16.1 ± 10.2 >0.05
Gender (% male) 117 (65%) 59 (49%) 0.009
Type II of diabetes 170 (94%) 96 (80%) 0.02
Insulin use 91 (51%) 58 (48%) >0.05
Previous ulcer 119 (66%) 31 (26%) 0.003
Chronic medical illness 108 (60%) 47 (39%) 0.005
Foot examination 14 (8%) 35 (29%) 0.002
Smoking 45 (25%) 25 (21%) >0.05
Low socioeconomic state 153 (85%) 82 (68%) 0.01
Ischaemia 125 (69%) 42 (35%) 0.004
Neuropathy 112 (62%) 46 (38%) 0.006
Renal insufficiency 32 (18%) 18 (15%) >0.05
Retinopathy 41 (23%) 22 (18%) >0.05

Values of age and duration of diabetes are mean ± S.D. Other values are number (%).
222 p r i m a r y c a r e d i a b e t e s 3 ( 2 0 0 9 ) 219–224

Table 2 – The main differences between group A and group B.

Group A Group B P value

Healed ulcer group Persistent ulcer or amputation group

(n = 111) (n = 69)
Age 56.2 ± 14.4 59.1 ± 11.3 >0.05
Duration of diabetes 9±7 16 ± 10 0.004
Gender (% male) 71 (64%) 46 (67%) >0.05
Type II of diabetes 106 (95%) 64 (93%) >0.05
Insulin use 33 (30%) 58 (84%) 0.001
Previous ulcer 75 (68%) 44 (64%) >0.05
Chronic medical illness 68 (61%) 40 (58%) >0.05
Foot examination 13 (12%) 1 (1%) 0.002
Smoking 27 (24%) 18 (26%) >0.05
Low socioeconomic state 92 (83%) 61 (88%) >0.05
Ischaemia 65 (59%) 60 (87%) 0.004
Infected ulcer 21 (19%) 59 (86%) <0.001
Neuropathy 67 (60%) 45 (65%) >0.05
Renal insufficiency 19 (17%) 13 (19%) >0.05
Retinopathy 24 (22%) 17 (25%) >0.05

Values of age and duration of diabetes are mean ± S.D. Other values are number (%).

disease, peripheral neuropathy and infection. However, there
has been no convincing evidence that these three factors are
the only important factors in the process of development
of diabetic foot ulceration. Other factors have been identi-
fied such as diabetes duration, type of diabetes, body weight,
anaemia, poor glycaemic control and others.
In this study, data obtained from all patients was evalu-
ated and all various expected risk factors for diabetic foot ulcer
were assessed. Male gender predominance is consistent with
many earlier studies like that of Edgar et al. [24] and Kiziltan
et al. [31]. It is possible to suggest that males are more liable
to foot trauma and hence they are commoner in diabetic foot
ulceration [35]. The average age in this study is younger to
that reported by Apelqvist and Agardh [21] and Boyko et al.
[36]; it may be due to the higher life span in Europe and U.S.
[37]. The reported average duration of the disease is higher
than the figures reported by Littzelman et al. [5] but consis-
tent with Oyibo et al. [20]. Although the present study together
with other studies like Boyko et al. [36], found that diabetes
duration was not related to the risk of developing foot ulcer,
some authors [17,24,38] found that this relation is statistically
significant.
Neuropathy and ischemia, two common complications of
diabetes mellitus, are the primary underlying risk factors
for the development of foot ulcers and their complications
[39]. This strong fact was confirmed by the current study.
Also, many other significant risk factors for diabetic foot
ulcer were identified. The results suggest that type II diabetes
mellitus, chronic medical illness and lack of frequent foot self-
examination are main significant risk factors.
Patients living in rural areas and those with poor socioe-
conomic conditions were at higher risk for the development
of diabetic foot ulcer. This result matches with many previous
studies like that of Chowdhury et al. [40] and Leymarie and
Richard [17]; the explanation may be that these patients are
less likely to take care of their foot problems.
From other studies, it is known that poor glycaemic
control and anaemia increases the risk of foot complica-
tions [24,36,38,41] this is well in line with our findings.
Nephropathy and retinopathy were not significant factors
in this study; the low prevalence of renal failure and eye
affection in our population possibly explain this lack of
significance.
The effect of greater body weight, insulin use and previous
history of foot ulcer on the development of foot ulceration is
controversial among literatures. Some studies show an associ-
ation between these factors and higher risk for foot ulceration
[36] and others deny this relationship [20,41]. The current
study did not find greater body weight and insulin use increase
the risk of diabetic foot ulceration, while past history of foot
ulcer seems to increase it significantly.
After classification of the patients into two groups accord-
ing to their outcome, the studied risk factors were reanalyzed
again to determine their impact on the outcome of the dis-
ease. The risk of an amputation or unhealed ulcer (group B)
increases with low haemoglobin and poor glycaemic control.
This finding is similar to that reported by Miyajima et al. [34].
Although longer duration of the disease and insulin treat-
ment were insignificant factors in the development of diabetic
foot ulcer, they are strongly related to the outcome as they
are associated more frequently and significantly with patients
in group (B). An evident relation was present between the
probability of amputation or persistent ulcer and vascular
insufficiency. These finding have been supported by many
studies like that of Reiber et al. [18] and Miyajima et al.
[34].
Both Armstrong et al. [22] and Adler et al. [23] found that
patients underwent surgery for lower extremity amputations
are more likely to have infected ulcers or sores. The same was
reported in the current study as the presence of infection was
significantly commoner in group (B) patients. In the same way,
Young et al. [16] reported that the relative risk of amputation
among the diabetic patients is highest among those who have
diabetic nephropathy but this does not match with our results
probably due to low percentage of chronic renal insufficiency
in the studied patients.
 p r i m a r y c a r e d i a b e t e s 3 ( 2 0 0 9 ) 219–224
Multiple risk factors exist along the continuum of condi-
tions and events leading to lower extremity amputation in
diabetes. Modification of certain risk factors by patients and
health professionals may reduce the risk for amputation and
thus decrease the human and dollar costs that accompany
limb loss in this prevalent chronic disease.
Conflict of interest
None.
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