Alsabek 2021

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Received: 13 April 2021 Revised: 13 June 2021 Accepted: 21 June 2021

DOI: 10.1111/iwj.13651

ORIGINAL ARTICLE

Diabetic foot ulcer, the effect of resource-poor


environments on healing time and direct cost:
A cohort study during Syrian crisis

Mhd Belal Alsabek1,2 | Abdul Razzak Abdul Aziz3

1
Al-Mouwassat University Hospital,
Faculty of Medicine, Damascus
Abstract
University, Damascus, Syria Diabetic foot ulcer (DFU) is one of the slowest healing wounds that hurt
2
Faculty of Medicine, Syrian Private the human body. Many studies from developed countries are concerned
University, Damascus, Syria
about materials, procedures, and equipment that accelerate the healing
3
Diabetic Foot Clinic, General Assembly
of Damascus Teaching Hospital,
time. In Sweden, the diabetic foot management costs around 24965
Damascus, Syria $/patient. In this review, we would evaluate the healing time of DFUs dur-
ing what is considered one of the worst humanitarian crisis of the 21st cen-
Correspondence
Mhd Belal Alsabek, MD, Al-Mazzeh St.,
tury. 1747 DFUs were studied from the main diabetic foot clinic in
P.O. Box 10989, Damascus, Syria. Damascus (2014-2019). We predicted many variables that could prolong the
Email: drsabekb@gmail.com healing time. The cost according to these variables was also reported. The
SINBAD Classification was performed to grade the severity of ulcers. We
noticed that the median healing time for DFUs was 8 weeks. Almost half of
these ulcers healed between 3 and 12 weeks. The time of healing for men
was significantly longer than that for women. While the presence of infec-
tion doubled the median time of healing, the presence of peripheral artery
disease doubled the mean of the direct health care cost. The location of the
ulcer acted as another independent risk factor. In conclusion, DFUs face
many barriers to heal during a crisis.The environment with resource-poor
settings should be added to the traditional risk factors that delay the
healing of DFUs for months or even years. More studies from disaster are as
are needed to evaluate low-cost materials that could be cost effective in
applying standard care of the diabetic foot.

KEYWORDS
diabetic foot infections, diabetic foot outcome, diabetic foot ulcers, healing time, peripheral
artery disease, plantar ulcer

Abbreviations: DF, diabetic foot; DFI, diabetic foot infections; DFUs, diabetic foot ulcers; IWGDF, International Working Group on the Diabetic
Foot; PAD, peripheral artery disease.
Abdul Razzak Abdul Aziz, MD, is the head of diabetic foot clinic in Damascus Teaching Hospital. D-Foot National Representative-Syria, Al-Mujtahed
St Damascus, Syria.

This is an open access article under the terms of the Creative Commons Attribution-NonCommercial License, which permits use, distribution and reproduction in any
medium, provided the original work is properly cited and is not used for commercial purposes.
© 2021 The Authors. International Wound Journal published by Medicalhelplines.com Inc (3M) and John Wiley & Sons Ltd.

Int Wound J. 2021;1–7. wileyonlinelibrary.com/journal/iwj 1


2 ALSABEK AND ABDUL AZIZ

Key Messages
• DFUs faced many barriers against the healing during the disaster
• the environment with resource-poor settings is the main barrier
• the healing time for DFUs in crisis areas is affected by many factors
• SINBAD score is an easy clinical classification to detect ulcer severity
• by this trial; predicting healing time becomes easier in (very) low-economic
countries

1 | INTRODUCTION debridement and minor amputation and the patient then


completed his/her management by scheduled appoint-
Foot ulcers are defined as lesions involving a skin break ments as an outpatient. Moreover, the lack of sources led
with loss of epithelium: they can extend into the dermis us to provide low-cost materials for dressing, footwear,
and deeper layers, sometimes involving bone and mus- and offloading. Here, we will also evaluate if these mate-
cle.1 Up to one-third of the half billion people with diabe- rials are useful and not wasting the time of the healing.
tes worldwide will develop a diabetic foot ulcer (DFU)
over the course of their lifetime. Over half of DFUs will
develop an infection. Of these, 17% will require an 2 | MATERIAL A ND METHODS
amputation.2
Adopting standard care to diabetic foot patient could This retrospective cohort study is based on electronic medi-
not be always affordable, especially in the crisis area. Per- cal record data from the Diabetic Foot Clinic in Damascus
forming training programmes for health care workers, Teaching hospital; the main hospital in Damascus, the capi-
providing healthy environments to protect DFUs from tal of Syria. It is considered the only tertiary referral diabetic
injuries, fighting the infectious agents, and reducing the foot clinic over the country. Orthopaedists, diabetologists,
amputation rates would be hard challenges in the third vascular and general surgeons used to refer diabetic foot
world countries.3 patients for consultation, radiological investigations, labs,
Furthermore, the financial burden of the complete and advanced interventions that could be required.
healing of the ulcer holds economic and social conse-
quences, and that is what many peer-reviewed studies
focus on. They worked on detecting variable factors that TABLE 1 SINBAD classification system and score

accelerate/prolong the healing time in every nation.4,5 Category Definition Score


From Arab nation countries, the PubMed Library has not Site Forefoot 0
included studies that concern about the healing time of
Midfoot and hindfoot 1
DFUs, the affecting factors, and the direct medical cost of
Ischaemia Pedal blood flow intact: at least 0
this process.
one palpable pulse
Clinical trials from Syria could play an important role
to clear the reality of how the societies during the disas- Clinical evidence of reduced pedal 1
flow
ters could face a big health issue like a DFU. Syria has a
two-tier health care: a national health system that is Neuropathy Protective sensation intact 0
applied by the government, which assumes fiscal and Protective sensation lost 1
administrative responsibility for the health care of all its Bacterial None 0
citizens, and a parallel system of private clinics and hos- infection Present 1
pitals offers services with extra amenities. At this point, Area Ulcer <1 cm2 0
the financial burden of diabetic foot care and manage-
Ulcer ≥1 cm2 1
ment is taken over by the government, patients, and
Depth Ulcer confined to skin and 0
(occasionally) the charitable organizations.
subcutaneous tissue
In the last decade, the whole Syrian health care sys-
Ulcer reaching muscle, tendon or 1
tem was severely harmed; the diabetic foot patients
deeper
(in particular) often could not able to be admitted in the
public hospital as inpatients. Alternatively, we applied in Total possible 6
score
our clinic a regional anaesthesia for all aggressive
ALSABEK AND ABDUL AZIZ 3

Data were collected for the following variables: Age who visited our clinic between January 2014 and
(which was defined as the age at first consultation at the December 2019. Of 2653 ulcers, we detected 2187 pri-
outpatient clinic), gender, DFU presentation date and mary/recurrent ulcers and 466 non-healing wounds
healing date (if applicable), infection, peripheral artery within 1 month after a minor amputation (amputation
disease (PAD), DFU location, and the severity of the limited to the foot), which were also identified as new
DFU at the presentation according to SINBAD classifica- ulcers. We excluded 92 and 538 DFUs that needed a
tion system. This classification system and the scoring major or minor amputation, respectively. Two hundred
are given in6 Table 1. ten ulcer patients were not able to be followed-up till
In our systematic practice, the patient used to under- complete healing because of either non-compliant
went full neurological and peripheral vascular evalua- patients (N = 202) or death by other medical prob-
tion. The 10-gmonofilament test is used to evaluate the lems (N = 8).
protective senses. The ankle brachial index was per- Data of simultaneous DFUs in one patient were also
formed as a measure for detecting the presence of PAD. removed (66 cases). The number of residual studied
The infection is detected mostly clinically and treated by ulcers was 1747. The ulcer was defined as “healed” when
antimicrobial agents. The ulcers were monitored by an a complete epithelialization was performed without dis-
experienced team every day, three times a week, or once charge, and there was no recurrence of the ulcer within
a week depending on the severity of the ulcer. The diam- 4 weeks following the registered date of healing.
eter (mm) and depth (mm) of each ulcer were a part of
monitoring and performed by a scale. The initial size
of the ulcer was taken after the primary debridement. 2.1 | Statistical analysis
Proper footwear, diabetic shoes, insoles, felted foam
technique, and total contact dressing were applied as Statistical analysis was performed using IBM Statistical
required. Package for the Social Sciences version 25 data analysis
This processing of diabetic foot care was divided into software.7 The data were explored for its completeness,
units for financial purposes (Table 2). We could recognise missing values, and outliers before the actual data analy-
a wide range between public and private services. The sis was performed. Descriptive statistical analysis was
prescription also had a variable cost and could not be performed for variables including demographic charac-
standard for every case. Lastly, we could note that the teristics and ulcer characteristics.
economic collapse in Syria has a heavy effect on the med- Descriptive statistics for the study population at base-
ical staff wage in the consultant and procedures units. line were calculated as median, mean, SDs, counts, and
The materials in the dressing and footwear prescription percentages. Non-parametric test was performed for the
sections adjusted the low-economic status, while the rela- continuous outcomes. The outcome of the time to healing
tively high cost of the imaging and interventional radiol- and categorical variables (Gender, age, SINBAD Classifi-
ogy was a reason to restrict their roles in the plan of the cation, infection, PAD, deformity, and location) was
management. examined with the use of the Mann-Whitney U test and
Retrospectively, we reviewed 2653 neuropathic/neu- Kruskal-Wallis one-way analysis of variance (ANOVA).
roischaemic DFUs in the charts of 1724 diabetic patients Mann-Whitney U test was used for independent variables

TABLE 2 Estimated unit costs (US $)

Resource use in outpatient clinic: Estimated unit cost


Clinic attendance (including nurse or consultant visit) (per week) 7$ (in average)
Angiogram One of these investigations per ulcer 115$
with PAD when the cost is affordable.
Computed tomography angiography 100$
Surgical procedures: Wide/Debridement (per ulcer) Mini = 5$/Max = 150$
Dressings and other consumables (per week) 18$
Prescribing: (antibiotics, opioids, supplements, etc.) (per week) Mini = 4$/Max = 400$
Footwear prescription:
Felted foam (for temporary offloading) (per plantar ulcer) 10$
Shoes/± soles (per ulcer) 20$
4 ALSABEK AND ABDUL AZIZ

TABLE 3 Association between categorical variables with healing time of neuropathic diabetic foot ulcers

Healing time (weeks)

Variables Frequency (%) Median Mean SD Mean rank P value*


Gender
Male 964 55.2 8.00 11.47 11.624 921.42 .000
Female 783 44.8 6.00 9.80 11.032 815.61
Age (years)
≥50 1505 86.8 8.00 10.82 11.499 870.02 .518
<50 228 13.2 8.00 10.08 10.681 847.09
SINBAD Classification
SINBAD score ≥3 768 44.0 14.00 16.34 13.714 1159.35 .000
SINBAD score ≤2 979 56.0 4.00 6.31 6.316 650.15
Presence of infection
Yes 553 31.7 12.00 14.78 12.863 1090.06 .000
No 1194 68.3 6.00 8.84 10.104 773.93
Presence PAD
With PAD 251 14.4 14.00 18.40 16.571 1191.03 .000
Without PAD 1496 85.6 6.00 9.43 9.696 820.81
Presence of deformity
Yes 130 7.4 12.00 13.70 10.507 1064.81 .000
No 1617 95.6 8.00 10.50 11.432 858.66
Location of wound
Plantar 581 34 10.00 13.56 13.094 977.39 .000
Non-plantar 1126 66 6.00 9.48 10.229 790.33

Note: Mann-Whitney U test.


Abbreviation: PAD, peripheral artery disease.
*
Statistically significant, P < .05.

with two groups while Kruskal-Wallis one-way ANOVA of 60.3 ± 11.1 years old. The mean age of every gender was,
was used to compare three or more independent vari- female: 61.0 ± 11.4 years old; male: 59.7 ± 10.9 years old.
ables. It was considered to have a statistically significant Mann-Whitney U test indicated that the healing time of male
difference with P < .05. (mean rank: 921.42; n = 946) was significantly longer than
female (mean rank: 815.61; n = 783), U = 331 688.500,
z = 4.374, P = .000, two-tailed.
3 | OUTCOME

The mean healing time for patients with a neuropathic 3.2 | SINBAD classification
DFU was 10.72 weeks while the median healing time
was 8.00 weeks. Among all DFUs, 49.5% (n = 864) healed We classified the 1747 DFUs according to SINBAD
within 3 to 12 weeks and 12.2% (n = 214) of them took classification system: Score 1: 28% (N = 489); score 2:
>20 weeks to be healed. In Table 3, we could find the fol- 28% (N = 490); score 3: 17.4% (N = 304); score 4:
lowing results. 17.7% (N = 309); score 5: 7.7% (N = 135); score 6:
1.1% (N = 20). It is clear that 44.0% of the sample sits
within SINBAD score ≥ 3, and longer healing time
3.1 | Demographic characteristics was significantly observed for DFU with SINBAD
score ≥ 3 (mean rank: 1159.35; n = 768) compared
This study involved 1410 patients (>18 years old) with neu- with DFU with SINBAD score <3 (mean rank: 650.15;
ropathic DFUs. Of the patients, 55.2% (n = 946) were male n = 979) U = 156 787.500, z = 21.010, P = .000,
and 44.8% (n = 783) were female, with an overall mean age two-tailed.
ALSABEK AND ABDUL AZIZ 5

3.3 | Infected ulcers vs non-infected 3.6 | The effect of DFU location in the
ulcers healing time

The incidence of the infection would be higher in an 3.6.1 | The healing time for plantar ulcer
unhealthy environment, which is more common in the
low socio-economic status, camps, and crisis areas such The location of the wound ulcer was also found to have a
as many of Syrian towns. We recorded DFUs as a DFI statistically significant relationship with the healing time
when the infection occurred in any stage of treatment: of the DFU. The test indicated that the healing time for
from the presentation till the healing. The study named patients with ulcers located at the plantar side of the foot
553 ulcers (31.7%) as an infected ulcer with healing time (mean rank: 977.39; n = 581) was significantly higher
(mean rank: 1090.06; n = 553) significantly longer than than the patients whose ulcers were not located at the
those with non-infected ulcer (mean rank: 773.93; plantar side of the foot (mean rank: 790.33; n = 1126)
n = 1194) U = 210 661, z = 12.223, P = .000. U = 255 414.5, z = 7.453, P = .000, two-tailed.

3.4 | The effect of PAD in the 3.6.2 | The anatomical region of DFUs
healing time
Kruskal-Wallis ANOVA indicated that there were signifi-
The recorded data mentioned 273 (15.6%) ulcers that cant differences between the healing times of DFUs
combined with a grade of PAD in the same lower extrem- according to anatomical region of foot: forefoot vs mid-
ity. Twenty-two of these cases underwent percutaneous foot or hindfoot. The median of healing time for forefoot
trans-luminal angiography and stenting or bypass. The was 6.00 while for midfoot or hindfoot was 12.00 for each
test indicated that the healing time for ulcers with PAD of them (Table 4). Other variables studied in this analysis
(mean rank: 1191.03; n = 251) was significantly higher were not statistically significant.
than the ulcers without PAD (mean rank: 820.81;
n = 1496) U = 108 173, z = 10.795, P = .000, two-
tailed. 3.7 | The direct health care cost to
achieve DFU healing

3.5 | The effect of deformity in the We could expect the direct health care cost of the DFU in
healing time of DFUs Syria (2014-2019) from the estimated unit costs (Table 3).
This cost had two divisions: (a) the fixed one, which
In this sample; there were 130 DFUs that were combined included the cost of vascular procedures, debridement
with variant types of foot deformity. Charcot foot was found cost, offloading, shoes, and soles. (b) The weekly cost,
in seven cases. The mean rank of healing time for these which depended on the duration of the healing time like
130 DFUs was 1064.81. It is clearly higher than those 1617 antibiotics, dressing, and clinical attendance. The cost of
DFUs without simultaneous deformity (mean rank: 858.66) achieving the complete healing of ulcer was studied in
U = 80 300, z = 4.498, P = .000, two-tailed. Table 5; the severity of the ulcer, PAD, infection, and

TABLE 4 Association between the wound anatomical region and healing time of diabetic foot ulcers

Healing time (weeks)


Variables
Wound anatomical region: Frequency (%) Median Mean Mean difference P value*
Forefoot Midfoot 1245 73.0 6.00 9.35 5.035* .000
Hind foot 6.751* .000
*
Midfoot Forefoot 240 14.1 12.00 14.38 5.035 .000
Hind foot 1.717 .235
*
Hind foot Forefoot 210 12.3 12.00 16.10 6.751 .000
Midfoot 1.717 .235

Note: Kruskal-Wallis one-way analysis of variance.


*
Statistically significant, P < .05.
6 ALSABEK AND ABDUL AZIZ

TABLE 5 Direct health care costs in US$ per ulcer

Direct health care costs to achieve healing per ulcer


Mean of healing Fixed Weekly
Number time (weeks) cost cost Mean SD Median P value*
Severity of ulcer (SINBAD)
SINBAD score ≥3 768 16.34 135 225 3810.59 3085.551 3285.00 .000
SINBAD score ≤2 979 6.31 60 50 375.73 315.812 260.00
Infected ulcer: 553 14.78 135 325 4939.48 4180.563 4035.00 .000
No infected ulcer 1194 8.84 135 50 576.92 505.191 435.00
Presence of PAD: 251 18.40 160 225 4299.64 3728.547 3310.00 .000
Without PAD 1496 9.43 60 225 2182.16 2181.604 1410.00
Plantar ulcer 581 13.56 95 225 3145.86 2946.247 2345.00 .000
Non-plantar ulcer 1126 9.48 85 225 2219.10 2301.581 1435.00

Abbreviation: PAD, peripheral artery disease.


*Statistically significant, P < .05/Mann-Whitney U test.

plantar position of ulcer played significant roles in provide high-quality shoes/soles to prevent incomplete
increasing the economic burden of DFUs. healing and early recurrence.
One of the limitations on studying the economic bur-
den of DFUs in low-income societies is the difficulty of
4 | DISCUSSION predicting the indirect cost, especially during a disaster or
crisis.
The wide variation of the diabetic foot cost between dif- The guidelines of IWGDF 2019 estimate the SINBAD
ferent countries was recorded in many published arti- scoring system a simple and quick classification to use; it
cles.4 While the expenses incurred as a total cost for has been validated for healing in diverse DFU
healing DFUs in Sweden was estimated around US populations, and has been shown to be acceptable to cli-
$24965/patient without amputation, the economic bur- nicians.10 This classification has been validated for both
den of DFUs in India showed expenses of US$1960 for ulcer healing and amputation prediction, presenting good
the treatment.8 These differences between the developed results, and has good reliability.11
countries and low-income countries (especially those that Diabetic foot complications may be disabling or even
suffer from disaster and crisis) could be explained by life-threatening, no doubt that the diabetic ulcer infec-
many factors. Firstly, the pay differentials among tions (DFI) are the major complications and play a main
health care workers between the two categories of role in slowing the healing.12 In our trial, DFI doubled
countries. Secondly, the developed countries usually the median of the healing time.
use the costly advanced equipment more frequently in PAD is present in approximately one-half of all patients
diagnosis, monitoring, and supporting the DFUs man- with foot ulcers.13 Although every diabetic foot classifica-
agement (eg, laboratories, MRI, nuclear bone scan, tion involves PAD as a predicting factor that combined by
angiogram, vascular procedures, revascularization, others to determine the risk of amputation and the chance
etc.).9 Also, materials that were used in the dressing, of healing, many studies suggest that PAD is considered as
offloading, and footwear are definitely not the same in an independent risk factor and DFUs with or without con-
the two categories of countries. Even though our trial comitant PAD should be defined as two separate disease
did not reach the diabetic foot inpatients, there is no states.14 The mild severity of PAD and the costly procedures
doubt that offering the full management care at the for revascularization were the main causes of lower num-
clinic succeeded in preserving hospital resources for bers of PAD patients (N = 22) who had been performed for
other emergency fields in crisis situation. revascularization procedures.
On the other hand, we noticed that shoes, soles, and The significantly prolonged time and high cost for the
their materials we have obtained in Syria for a long time do healing of plantar ulcer are an index for the necessity of
not achieve the complete healing in the time and increase improving materials that support accelerating the
the rate of early recurrence of neuropathic DFUs (within healing. The cost-effective approach of using inexpensive
4 weeks). We could say that the cost of these materials materials did not encourage us to recommend it as ideal
would not be effective and the medical society should materials.
ALSABEK AND ABDUL AZIZ 7

5 | C ON C L U S I ON 3. Aziz ARA, Alsabek MB. Diabetic foot and disaster; risk factors
for amputation during the Syrian crisis. J Diabetes Complica-
DFUs face many barriers against healing during a crisis. tions. 2019 Feb;01:107493.
4. Tchero H, Kangambega P, Lin L, et al. Cost of diabetic foot in
The environment with resource-poor settings should be
France, Spain, Italy, Germany and United Kingdom: a system-
added to the traditional risk factors that delay the healing atic review. Ann Endocrinol (Paris). 2018;79(2):67-74. https://
of DFUs for months or even years. doi.org/10.1016/j.ando.2017.11.005.
In addition, this clinical trial adds another proof that 5. Toscano CM, Sugita TH, Rosa MQM, et al. Annual direct medi-
SINBAD Classification predicts the outcome of DFUs. cal costs of diabetic foot disease in Brazil: a cost of illness study.
More studies from disaster areas are needed to evaluate Int J Environ Res Public Health. 2018;15:89.
and suggest more affordable materials that are helpful in 6. Ince P, Abbas ZG, Lutale JK, et al. Use of the SINBAD classifi-
cation system and score in comparing outcome of foot ulcer
applying standard care and management in the diabetic
management on three continents. Diabetes Care. 2008;31:964-
foot field.
967. https://doi.org/10.2337/dc07-2367.
7. Corp IBM. IBM SPSS Statistics for Windows, Version 25.0.
CONFLICT OF INTEREST Armonk, NY: IBM Corp; 2017.
The authors report no commercial or other association 8. Alok Raghav ZAKRKL, Jamal A, Mishra SN. Financial burden
that might pose a conflict of interest with respect to this of diabetic foot ulcers to world: a progressive topic to discuss
clinical trial. always. Ther Adv Endocrinol Metabol. 2018;9(1):29-31.
9. Kerr M, Barron E, Chadwick P, et al. The cost of diabetic foot
ulcers and amputations to the National Health Service in
A U T H O R C ON T R I B U T I O NS
England. Diabet Med. 2019;36(8):995-1002.
Mhd Belal Alsabek: Attending Surgeon at Al-Mouwassat 10. Monteiro-Soares M, Russell D, Boyko EJ, et al. International
University Hospital, corresponding author, collected the Working Group on the Diabetic Foot (IWGDF) guidelines on
data, wrote the manuscript, and analysed the data statisti- the classification of diabetic foot ulcers (IWGDF 2019). Diabetes
cally. Abdul Razzak Abdul Aziz: General and diabetic Metab Res Rev. 2020;36(Suppl. 1):e3273. https://doi.org/10.1002/
foot surgeon. The head of diabetic foot clinic in Damascus dmrr.3273.
Teaching Hospital. D-Foot National Representative-Syria. 11. Forsythe RO, Ozdemir BA, Chemla ES, Jones KG, Hinchliffe RJ.
He supervised the management of the patients in the sam- Interobserver reliability of three validated scoring systems in the
assessment of diabetic foot ulcers. Int J Low Extrem Wounds.
ple during the 5 years of the trial, offered the plan of the
2016;15:213-219. https://doi.org/10.1177/1534734616654567.
treatment, supervised the clinical trial, and reviewed the 12. Seth A, Attri AK, Kataria H, Kochhar S, Seth SA, Gautam N.
manuscript. All the authors made an equal contribution to Clinical profile and outcome in patients of diabetic foot infec-
the creation of the presented clinical trial. tion. Int J Appl Basic Med Res. 2019;9:14-19.
13. Prompers L, Huijberts M, Apelqvist J, et al. High prevalence of
DATA AVAILABILITY STATEMENT ischaemia, infection and serious comorbidity in patients with
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Eurodiale study. Diabetologia. 2007;50:18-25.
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ORCID ferences between individuals with and without peripheral
Mhd Belal Alsabek https://orcid.org/0000-0001-6746- arterial disease. The EURODIALE study. Diabetologia. 2008;51:
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