Research Article
Direct Inflicting Causes of Diabetic Foot Ulcer & the Initial Action of Patient & Health Provider
Siddig Ad-DawAlshareef1 and Mohamed Elmakki Ahmed1,2*
1Department of Surgery, Jabir Abu Eliz Diabetic Centre, Khartoum, Sudan,
2Department of Surgery, University of Khartoum, Sudan
*Corresponding author: Mohamed El Makki Ahmed, Department of Surgery, Jabir Abu Eliz Diabetic Centre, Khartoum, Sudan
Published: 25 Apr, 2017
Cite this article as: Ad-DawAlshareef S, Ahmed ME. Direct
Inflicting Causes of Diabetic Foot Ulcer
& the Initial Action of Patient & Health
Provider. Clin Surg. 2017; 2: 1432.
Abstract
Background: The role of neuropathy and angiopathy in the causation of the diabetic foot are well
established. The purpose of this study is to investigate the effects of direct precipitating causes of
diabetic foot ulcer and the initial action of patient and primary health provider on outcome of DFU.
Patients and Method: This prospective study was conducted in Jabir Abu Eliz Diabetic Centre
(JADC), Khartoum, Sudan. Recorded data included patient’s demographics, DFU direct inflicting
cause, initial behaviour of the patient, information related to the 1st health provider, and outcomes.
Results: A total of 134 patients who had diabetic foot ulcer (DFU) were included. The mean age of
the studied patients was 56.78 ± SD 10.2 years with a male to female ratio (4.6: 1). The mean duration
of DFU was 36 ± SD 97 days. Neuropathy and angiopathy were reported in 76.9% and 25.3% of
patients respectively. Grade of infection was significantly associated with foot self-examination
(p=0.006), and duration of DFU (p=0.032). The common direct causes of foot ulcer were blister
(28.4%), penetrating injuries / sharp injuries (23.1%), and unidentified causes (22.4%). Outcome
of ulcer was significantly associated with direct precipitating causes of DFU (p=0.033), level of
1st health provider (p=0.000), and the action of 1st health provider (p=0.007). Major lower limb
amputation and chronic ulcers were encountered in ulcers precipitated with ill-fitting shoes/socks
or penetrating / sharp injuries, seen by physicians, and treated with antibiotics after sever sepsis.
Conclusion: The most direct precipitating causes of DFU are avoidable. Presentation of DFU is
affected with patient behaviour and delay in presentation to JADC. We recommend developing
a community intervention programme to increase the awareness among diabetic patients and
encourage earlier multidisciplinary team assessment to reduce disparities and improve foot
outcomes in patients with diabetes.
Keywords: Diabetic foot ulcer; Inflicting causes; Major lower limb amputation
Introduction
Foot ulcers rarely result from a single pathology; instead many overlapping factors lead to foot
ulceration. They put the foot at risk, precipitate a break in the skin, or impair healing [1-4]. Those
factors that put the foot at risk like peripheral neuropathy, peripheral vascular disease, limited joint
mobility, and deformity are well-studied [1,3,5-8]. On the other hand little is known about the exact
precipitating factors and their impact on the presentation and outcome of the DFU.
There have been few studies of psychosocial factors in the pathway to ulcers and the impact of
the patient behaviour on the presentation and outcome of the DFU Vileikyte [9]. Few studies were
done to evaluate if the level of, and the initial management modality undertaken by the first healthcare
professional will affect the presentation and outcome of the DFU.
The vast majority of diabetic foot ulcers were attributed to inadequate footwear in the western
communities [10-12]. In Africa the nature of the precipitating causes of the DFU were undefined
most of times [11,13]. Widatallaand his colleagues in 2009 reported no inflicting cause were
identified in the majority of the patients in Sudan [14]. Studies from USA and UK indicate that
39–76 percent of amputations were similarly initiated by ill-fitting footwear [15,16]. The relation
between the precipitating factors of the diabetic foot ulcer and outcome needs to be clarified in the
developing countries.
The aim of this study was to see the effects of direct inflicting causes of the diabetic foot and the
initial action of the patient and primary health provider on outcome of DFU.
Table 1
Table 2
Patients and Methods
This was a prospective study done among patients with DF
attending Jabir Abu Eliz Diabetic Centre (JADC) Khartoum, between
April 2013 and April 2014. JADC is a multidisciplinary polyclinic
established in1998. The center offers outpatient medical, surgical,
ophthalmic, dermatological and dental care with supportive services
in prophylactic foot screening, offloading and shoe-making factory.
The centre receives 300- 350 patients with diabetes daily, of whom
about 150 patients with diabetic foot with an average of 10 -20 new
cases with diabetic foot seen daily.
143 patients with DF attending JADC were studied. Treatment
included surgical, debridement and removal of callus and necrotic
tissue, antibiotics given empirically and later on culture and
sensitivity and off-loading as required. Patients with clinical evidence
of ischemia were seen by the vascular surgeon.
The degree of infection was assessed using the Wagner
classification and System Staging System classification [17,18].
Somatic sensory neuropathy was assessed by the 10g (Semmes–
Weinstein) monofilament and a 128 Hz tune fork insensitivity at
hallux [19,20]. Ankle-brachial index (ABI) was used to assess the
peripheral arterial disease (PAD) and was considered compatible
with ischemia when lower than 0.9 [21].
All patients were followed as required up to 6 months. Patient’s
attitude towards his foot was assessed by reporting if the discovery of
DFU was by the patient himself or by other person. The immediate
reaction of the patient toward his/her DFU after discovery and
duration from the time of injury to the presentation at JADC in
Khartoum.
Statistical analysis
We used the statistical package for social sciences (IBM SPSS)
for Windows version 22.0 statistical software (SPSS Inc., Chicago, IL,
USA).
Chi-square tests were used to assess the association between the
precipitating causes of DFU, patient behaviour, and first health-care
professional variables and the presentation and outcome of the DFU.
Another multinomial regression analysis was performed to assess
which variables were independently associated with the presentation
and outcome of the DFU. The statistical significance was defined as
a P value < 0.05.
Results
One hundred thirty four patients with diabetic foot ulcer were
included. The mean age was 56.78 ± 10.2 years. Male to female ratio
was 4.6: 1.0. The majority of patients were resident in Khartoum state
(61.2%) and the rest were coming from different regions. Almost half
of the sample were hard labour (52.2%) and of low socio economic
status (59%). More than half of patients were wearing regular
footwear (n=89, 66.4%), thirty seven patients (27.6%) used special
diabetic footwear, and eight patients (6%) were bear feet during the
injury.
The mean duration of diabetes was 13 ± 8 years. Majority of
patients (n=118, 88.1%) were Type 2 DM. 58.2% are on insulin, 39.6%
on oral hypoglycaemic drugs, and 2.2% on diet. Forty eight patients
had previous DFU. Twenty nine patients (60.4%) healed without
amputation Thirteen patients (27.1%) healed with minor amputation,
and 6 (12.5%) ended with major lower limb amputation.
According to the Wagner classification 16 patients were grade1
(11.9%), 49 patients were grade 2 (36.6 %), and 46 patients were grade
3 (34.3%).According to the simple staging system classification 18
patients were grade 1(13.4%), and 56 patients were grade 2 (41.8%)
(Table 1).
One hundred and three patients (76.9%) had neuropathy as tested
by 10 gram monofilament test. ABI were more than 1.3 in 16 patients
(11.9%), normal 1.3–0.9 in 84 patients (62.8%), mild ischemia 0.8 in
33 patients (24.6%) and sever ischemia in one patient (0.7%).
The most common direct causes of foot ulcer were blister (28.4%),
followed by penetrating injuries/sharp injuries (23.1%) (Table 2).
Wagner classification grades 1 and 2 collectively were 61.29% in
ulcers precipitated with penetrating/sharp injuries, 50% in ill-fitting
shoes/socks, 43.4% in undefined cause, and 42.1% in blister. There
were no significance association between the grade of infection and
precipitating cause of DFU (p-value = 0.860).
Healing was achieved in 92.1% of ulcers precipitated with blister
and 83.8% of penetrating/sharp injuries. Chronic ulcers were mainly
precipitated with penetrating/sharp injuries (12.9%) and blister
(7.89%). Major lower limb amputation were mostly encountered
in ulcers precipitated with ill-fitting shoes/socks (36.36%) and
undefined cause (33.33%) (p=0.033) (Table 3). The majority of
patients discovered their foot lesion by themselves (n= 120, 89.6%)
and the rest by another member (n=14, 10.4%). Wagner classification
grades 3, 4 and 5 collectively were 46.67% in patients discovered their
foot lesion by themselves, and 92.9% in those discovered by other
person (p-value =0.005).Major lower limb amputation was 14.17%
in patients discovered their foot lesion by themselves, and 21.43% in
those discovered by other person (p-value = 0.674).
One hundred and three patients (76.9%) reported to health
facilities, 24 patients (17.9%) had traditional treatment, and 7 patients
(5.2%) did not seeking treatment. There are no difference between the three groups regarding the grades of Wagner classification and
outcome of DFU in the study group (p-value = 0.811). The mean
duration from time of injury to presentation to JADC was 36 ± 97
days. The chances for presenting with advanced grade of infection
by SSS classification were increased by 1 for every single day delay
in presentation to JADC (p-value =0.022). There was statistically
significant relationship between this duration and the grade of
infection by Wagner classification (p-value =0.032), and SSS
classification (p-value =0.003).
The level of 1st health provider was a junior doctor in 40 patients
(29.9%), medical assistant/nurse in 36 patients (26.9%), surgeon
specialist in 35 patients (26%), and non- surgeon specialist in 23
patients (17.2%). There are no difference between the four categories
regarding the grades of Wagner classification of DFU in the study
group (p-value = 0.905). Healing were achieved in 91.43% of ulcers
firstly seen by surgeon specialists, 75% in junior doctors, 69.44% in
medical assistants0/nurses and 65.22% in non- surgeon specialists.
Major lower limb amputation were mostly encountered in patients
firstly seen by junior doctors (20%), followed by non- surgeon
specialists (17.39%), medical assistants/nurses (16.67%) and at last
surgeon specialists (5.71%). Chronic ulcers were mainly seen by nonsurgeon
specialists (13.04%) and medical assistants/nurses (11.11%).
The level of the 1st health provider have statistically significant
relationship with the outcome and strong impact on it (p-value
=0.000).
The action taken by the 1st health provider toward the DFU was
surgical treatment in 87 patients (64.9%), antibiotic and supportive
management in 35 patients 26.1%, and referral to a surgical specialist
in 12 patients (9%). Grades 3, 4 and 5 by Wagner classification were
collectively 52.87% in patients treated firstly by surgical treatment,
51.43% in antibiotic and supportive management group and 41.67%
in those referred to a surgical specialist (p-value = 0.903). Healing
was achieved in 82.78% of patients firstly treated by surgical
treatment, 66.67% in patients referred to a surgical specialist and
62.85% in antibiotic and supportive management group. Major
lower limb amputations were mostly encountered in patients treated
with antibiotic and supportive management (28.57%). The effect of
behaviour of health-care professional have statistically significant
relationship with the outcome (p-value=0.007).
The mean duration of healing of DFU in the study group was 132
± 115 days. Sixty four patients (47.8%) healed without amputation.
Thirty eight patients (28.4%) healed with minor amputation. Twenty
patients (14.8%) ended with major lower limb amputation, 10
patients (7.5 %) developed chronic ulcer, and 2 patients died (1.5 %).
Both deaths were male (48 & 52 years old), Type 2 diabetes mellitus
with no comorbidity. Their injury were precipitated with ill-fitting
shoes/socks and undefined cause. Both had exposure to private
diabetic centre and presented to JADC after more than 2 weeks from
the initial injury. They died from sever sepsis.
From the above analysis of precipitating cause of DFU, behaviour
of patient toward his/her DFU, level of first health-care professional,
and behaviour of health-care professional we found the following:
If the DFU was precipitated by blister, discovered by the patient,
the duration from time of injury to presentation to JADC < 2 weeks,
the first health-care professional is surgical specialist and he treated
the ulcer with surgical management this will result in healing.
If the DFU was precipitated by ill-fitting shoes/socks, discovered
by other person, the duration from time of injury to presentation to
JADC >2 weeks, the first health-care professional is non-surgeon
specialist and he treated the ulcer with antibiotic and supportive
management this will result in major lower limb amputation.
If the DFU was precipitated by penetrating/sharp injuries, the
first health-care professional is non-surgeon specialist and he treated
the ulcer with antibiotic and supportive management this will result
in chronic ulcer regardless the duration from time of injury to
presentation to JADC.
Table 3
Discussion
In this prospective observational study of one hundred thirty
four patients with diabetic foot ulcer were included. Patients were
predominately male and had Type 2 diabetes. Male to female ratio
was [4.6: 1] which is similar to other study [11,22,23]. This is because
males are more prone to trauma and have less foot care.
The mean age in our study (56.7±SD10 years) is in accordance to
Widatalla “et al.” [24] (56.7 ± SD11 years), and to what was reported
by Doumi in Western Sudan (56.8 ± SD12 years) [25]. But it is
occurred in older age in UK (66.1 ± 15.1) [23].
The mean duration of diabetes was 13 ± 8 years. Morbach “et al.”
(11) Found a significantly long mean duration of diabetes among
German (14.0 ± 10.8 years) and Indian (11.7 ± 7.1 years) patients than
among Tanzanian patients (5.1 ± 4.8 years) [26]. This finding may
imply the differences in the quality of diabetes care where German and
Indian patients, on average have longer duration of diabetes exposure
before they develop foot ulcers. This similarity to our finding may be
explained by that 35.8% of patients had past history of DFU. And they
presented with shorter duration of diabetes at their first DFU.
This study showed higher prevalence of neuropathy (76.9%)
when compared to angiopathy (25.3%). This is similar to the reports
from developing countries where ischemic disease accounts for only
20–30 % of cases [11,27-30]. In contrast, Western Europe and the
USA, although reporting high prevalence of neuropathy, but show
prevalence of ischemic disease usually between 40 and 50 % or
more [23,31-33]. The high prevalence of obesity and consequently
atherosclerotic disease as well as older mean age and possibly higher
rates of smoking in the population from developed countries place
diabetic individuals at higher risk for ischemic disease.
The vast majority of diabetic foot lesions (DFL) were attributed
to inadequate footwear in the western communities [10-12]. In our
study blisters (28.4%), penetrating injuries/sharp injuries (23.1%),
unidentified causes (22.4%), and ill-fitting shoes/socks (16.4%)
represent the most common direct cause of foot ulcer in this study.
In their study in, Ogbera et al from Nigeria reported similar
figures where spontaneous blisters (26.5%) and unidentified causes
(21.2%) were the most common precipitating factors for DFL [13].
Similarly, unidentified causes were found to represent 22% of the
causes of DFL in Tanzania [11]. In a study done at JADC, Widatalla
et al found no inflicting cause were identified in the majority of the
patients (40.4%). Sharp injuries were reported in 17.8 % [14]. This
reduction in the unidentified group may be explained by the growing
prevalence of diabetes mellitus and DFU.
Our study reveals statistically significant relationship between
the precipitating cause of DFU and outcome. The most favourable
outcome seen in ulcers precipitated with blister (healing achieved
in 92.1%) which is the first common direct cause of DFU. Blisters
represent fluid filled cavities that develop usually at the sites of
increased pressure and represent a closed ulcer. The high incidence of
blisters in the studied population might be due to the high incidence
of neural impairment, foot deformity leading to dry skin, fissuring
and callosities. These blisters also may be the predisposing factors in
the “unidentified group” as they represent ports of entry for bacteria
leading to infection without obvious preceding agent.
Major lower limb amputation was mostly encountered in ulcers
precipitated with ill-fitting shoes/socks (36.36%). This finding is
in accordance to other studies that indicate that 39–76 percent of
amputations were similarly initiated by ill-fitting footwear [15,16].
Chronic ulcers were mainly precipitated with penetrating/sharp
injuries (12.9%). Penetrating injuries were the second most common
precipitating factors. The impaired visual acuity of the diabetic
population, the absence of night illumination in most of the country,
the dry hot weather, and the agricultural nature of the Sudan which
make open light shoes a convenient accommodation may be the main
factors in its causation.
Previous studies have indicated that diabetic patients were up to
46 times more likely to have an amputation after a puncture injury
compared with patients without diabetes [34-36]. Lavery et al reported
that as many as 41% of puncture injuries in persons with diabetes
occur while the patient is not wearing shoes [36]. This in contrast to
our finding were 27 patients had penetrating/sharp injuries (83.7%)
wearing regular footwear and 8 of them special diabetic footwear
at the time of the injury. This finding may reflect that the special
diabetic footwear available in the markets is not protective against
the precipitating cause of DFU in the study group. Most of the special
diabetic footwear available in the markets is designed for the western
nations.
The evidence from this survey indicates that the majority of the
patients discovered their foot lesion by themselves (89.6%) in spite
of the high percentage of neuropathy (77.6). Both Wagner grade and
major amputation were higher in those with sever neuropathy when
the injury was discovered by a relative compared to those who felt the
injury. This may be attributed that most of our patients are Muslims
and they wash their feet as part of preparations for pray 5 times per
day. Macfarlane “et al.” [12], reported that about 50% of diabetic
patients were unaware of their foot ulcers.
Our study revealed that the discovery of DFU by the patient is
more protective against presentation with advanced grade of infection.
Margolis “et al.” [37] in study published in 2014 noted the minimal
effect of patient foot self-examination on decreasing the rate of lower
extremity amputations. A similar observation was made previously
in a group of patients treated in the Veterans Administration system,
USA [38,39].
This study also showed that the mean duration from time of injury
to presentation to JADC was 36 ± 97 days. During this period most
of patients received medical care by different health care personnel.
This is in contrast to what have been reported from UK [12], where
the average delay was only 4 days, and to what have been reported
from Algeria [28], which was 31 days. Our study reveals significant
relationship between this duration and the grades of infection. This
delay may be due to lack of clear referral system in Sudan. Another
reason is the majority of the sample was less educated about diabetes
(regarding the importance of general foot care, the significance of
diabetes and its complications), and from low socioeconomic level.
Margolis “et al.” [37] reported that areas with more diabetes based
education reported lower rates of lower extremity amputations.
A qualitative study by Feinglass and his colleges in 2012 concluded
that patients with low or marginal health literacy misunderstood the
gravity of their medical history with respect to the onset of their lower
extremity amputations [40].
Few studies tried to assess the behaviour of patients towards
their foot lesions. This study showed that the general care of diabetic
patients towards their DFL is sub-optimum. They either ignored their
lesions completely or tried some local remedies mostly in the form
of herbal medicines or honey. Even for those who sought medical
advice for the control of their lesions, a considerable proportion went
to junior doctors or medical assistants/nurses, who are generally not
well-qualified in Sudan.M
Different caregivers in this study provided different kinds of
management to the DFU, with the surgeons being most likely on the
right track. Junior doctors and medical assistants/nurses constituted
56.8% collectively of the1st health providers for the sample. This may
be attributable to the lack of a national protocol to treat DFU. The
most favourable outcome was achieved when patients initially seen by surgeon specialists and referred to specialized diabetic centre.
The most unfavourable outcome percentage were seen in the
category of non- surgeon specialists (34.78%) followed by medical
assistants/nurses (30.56%), and junior doctors (25%). The effects
of level of the 1st health provider have statistically significant
relationship with the outcome and strong impact on it. These findings
confirm what Ndip and his colleges in 2006 reported that physicians
never examined the feet of 86% of diabetic patients [41]. However, it
was Paul Brand (1914–2003) who added science to the art of foot care
[42-44]. When he spoke at a US Department of Health conference
and was asked to make a recommendation on reducing amputation
in diabetes, most listeners expected an answer promoting vascular
surgery or modern medications. They were surprised to hear that
his key recommendation was a national campaign to encourage
physicians to remove patients’ shoes and socks and to examine the
feet [42,45].
This study shows significant statistical relationship between
the action taken by the 1st health provider toward the DFU and
the outcome DFU. Among ulcers that healed without amputation;
surgical treatment was the modality of treatment in 73.44% of all
ulcers with same outcome. Also in ulcers that healed with major
amputation antibiotic and supportive management was the modality
of treatment in 50% of all major amputations. This finding is
consistent with reports from other studies that surgical treatment is
essential in healing a diabetic ulcer [46-50].
Piaggessi “et al.” [51]. reported that surgical treatment of
neuropathic foot ulcers in diabetic patients proved to be an effective
approach compared to conventional treatment in terms of healing
time, complications, and relapses, and can be safely performed in
an outpatient setting. Also Brem and his colleges [52] reported that
antibiotics may be useful to treat superficial infections, but they
are often not sufficient to heal chronic wounds and, specifically,
uncomplicated diabetic neuropathic forefoot ulcers [46,53].
Healing without amputation was the most common outcome of
DFL (47.8% of DFL). The percentages of patients who ended with
minor amputation or major lower limb amputation were 28.4%, and
14.8% respectively. Our study reflect better outcome in comparison to
what reported from Western Sudan. They reported 24.7% of patients
ended with major lower limb amputation [25]. The mortality in this
study was 1.5%, a much better figure than what was reported twenty
eight years ago from Khartoum Teaching Hospital, where a mortality
of 22.1% was reported [54]. These findings reflect the high quality
of care which patients received with multidisciplinary polyclinic
activities in JADC [55-60].
Chalya and his colleges in 2011 reported that a multidisciplinary
team approach targeting at good glycaemic control, education on
foot care and appropriate footwear, control of infection and early
surgical intervention is required in order to reduce the morbidity and
mortality associated with DFUs [50].
Finally in spite of the prevalence of neuropathy and angiopathy;
this study showed that 77.6% of DFU were precipitated with
identifiable and preventable causes. Pecoraro “et al.” [5] reported that
many amputations in diabetic patients were potentially preventable,
and that minor trauma, neuropathy, ischemia, and infection were
major contributory factors in the causal chain that ultimately resulted
in amputation. Defining causal pathways that predispose to diabetic
limb amputation suggests practical interventions that may be effective
in preventing diabetic limb loss [61-65].
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