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Effectiveness of Honey in treatment diabetic foot ulcer : a systematic review

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 EFFECTIVENESS OF HONEY IN TREATMENT OF DIABETIC FOOT ULCER: A
SYSTEMATIC REVIEW

Muhammad Saleh Nuwa, Galih Noor Alivian, Julvainda Eka Priya Utama, Anita
Fatarona
Faculty of Nursing, Universitas Airlangga
Email: musa.nuwa@gmail.com

ABSTRACT
Introduction: Honey has been known for thousand years for its effects on wound healing
process. Honey has antibacterial characteristics, stimulates the release of cytokines, and
stimulates cellular growth, so that it can facilitate wound healing process. Diabetic Foot Ulcer
(DFU) is one type of wounds which is its wound healing process still becomes problem. The
purpose of this systematic review was to determine the effectiveness of honey in healing
diabetic foot ulcers. Method: The process of searching articles conducted on 7 database to
answer the purpose of this review. There was 7 of 10 articles discuss about wound care with
honey using RCT design. 5 of 10 articles was high quality articles with medium level of
recommendations, 2 articles were medium quality articles with medium level, and 3 articles
used cohort design with a high quality medium level. Result: Several articles have been
reviewed and it is known that honey is a good alternative choice in wound care of DFU.
Conclusion: Meanwhile, to conclude that honey is one of the best alternatives in wound care
requires a lot of randomized clinical study which compares honey with a variety of existing
topical agents.

Keywords: Honey, diabetic foot ulcer, wound care

INTRODUCTION per 1,000 patients with diabetic ulcers

Diabetic Foot Ulcer (DFU) is one of
the long-term complications of diabetes
mellitus with risk of death by 25%.
Approximately 15% of individuals with
diabetes mellitus will suffer from diabetic
foot ulcers (Deribe, 2014). Centre for
Disease Control and Prevention reported
that in 2003 about 11.6% of people in
United States suffer from DFU, and in the
same year in UK found about 7.4% of
patients suffering from the same disease.
This amount will continue to increase along
with unhealthy lifestyle of people (Zubair,
2015). Another study mentioned that about
38% of all amputations in United States was
related to DM disease (Dinker R Pai, 2013).
Data from WHO showed the rate of
amputations in patient with diabetes usually
10 to 20 times that from non-diabetic
patients. Over the last decade, rate of
amputations increased by 1.5 to 3.5 events
(World Health Organization, 2016).
Meanwhile, according to the report
from RISKESDA (2013), the prevalence of
diabetes which diagnosed by doctors was
2.1%. Those prevalence is higher than in
RISKESDA (2007) which is about 1.1%.
There are some provinces which have
higher prevalence than the national average,
that is Central Sulawesi (3.7%), North
Sulawesi (3.6%), South Sulawesi (3.4%)
and East Nusa Tenggara 3.3%. The
prevalence of diabetes tends to be higher in
women than in men and is more common in
urban communities ( DEPKES RI, 2013).
Unlike in Western countries, in Indonesia
there are only a few studies about the
prevalence and factors associated with
DFU. The main complications of DM in
Indonesia is neuropathy (13% - 78%), micro
vascular complications (16% - 53%) and
DFU (7,3% - 24%) (Yusuf et al., 2016).

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8th International Nursing Conference “Education, Practice And Research Development In Nursing”
 A patient with DFU tend to
experience symptoms including pain,
limited mobility, pruritus, sleep
disturbances, leakage and malodor of
exudate in the wound, and there are some
psychological effects such as emotions,
embarrassment, frustration and self-esteem
becomes reduced. (Harding et al., 2016).
Many studies have been done to prevent
further complication of DFU, one of which
is good wound care. One of the topical agent
which is known over the centuries as topical
medication for variety of wounds, including
the methods of modern wound care is honey
(Vandamme, Heyneman, Hoeksema,
Verbelen, & Monstrey, 2013).
Honey has been known for
thousands of years for its effect on wound
healing process (Lindberg, Andersson,
Palm, & Fagerström, 2015). Honey has
multiple effects on the wound. In vitro and
animal studies showed that honey has
antibacterial characteristics, stimulates the
release of cytokines, and stimulates cellular
growth, so that it can facilitate wound
healing process (Jull, Walker, Parag,
Molan, & Rodgers, 2007). There are many
studies that have studied about the effects of
honey in treating DFU but not many of
which using systematic review method.
This systematic review aimed to evaluate
objectively the effectiveness of honey in
wound care (Diabetic Foot Ulcer) in
patients with DFU using existing research
evidence.
METHOD
Article search
The first step in this scientific article
search was to formulate PICOT Framework
(P: patients who suffer from DFU, I: all
wound care interventions which use honey
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8th International Nursing Conference “Education, Practice And Research Development In Nursing”
or raw materials of honey, C: Topical agents
other than honey, O: effectiveness in DFU
healing, T: duration of wound healing). So
that, the formulation of this research
questions was “How is the effectiveness of
honey in treatment of diabetic foot wound
(Diabetic Foot Ulcer) in patients with DFU?
Furthermore, the database used in
this study was CINAHL Ebsco, Sage
Journal, Science Direct, Google Scholar,
and Proquest which is limited to articles in
English published from 2000 to 2016.
Searches were conducted in September until
November 2016. Keywords to search
literature included wound care, diabetic foot
ulcers, honey, wound care with honey,
diabetic wound, and honey in wound care.
Inclusion and exclusion criteria as
determined before literature search started.
Inclusion criteria were: (a) primary research
articles about wound care using honey in
patients with DFU (b) full-text articles.
Exclusion criteria were (a) articles which is
not in English (b) articles which discuss
about wound care besides DFU (c) articles
which is contain no abstract and (d) articles
which discuss about wound care in animal
experiments. Articles were selected by the
researcher in terms of keywords which is
correspond to the search of electronic
databases, and then researcher determine
whether the inclusion criteria is reached,
followed by a review of full-text version. A
total of 1679 articles found, 510 articles of
which discuss about wound care using
honey. Articles which is appropriate with
the inclusion criteria and were reviewed as
many as 10 articles. Schematically, it can be
shown in following PRISMA diagram
(Preferred Reporting Items for Systematic
Reviews and Meta-Analyses):
 Articles from the database: Articles based on keywords :
CINAHAL Ebsco, SAGE Journal, wound care, diabetic foot ulcer,
Google Scholar, Science Direct, and honey, wound care with honey,
ProQuest 2006-2016 (n = 1679) diabetic wound, and honey in wound

Articles that has been screened: Article based on exclusion criteria:

(n = 510) (n=500)

Article based on inclusion criteria: 10 articles selected

n = (10)
Figure 1. Article Meta-analysis

Quality and level assessment of articles
Researcher conducted critical
appraisal using tools from The Joanna
Briggs Institute Critical Appraisal tools for
use in JBI Systematic Reviews for all
articles that have been selected. All articles
were assessed with tools which is
appropriate with its research design (The
Joanna Briggs Institute, 2016). Then,
resercher conducted an assessment of the
quality of each article which depends on the
method used and existing designs. There
was high quality (80-100)%, medium
quality (70-79)% and the low quality
articles <69%. Furthermore, researcher
conducted the assessment of the quality and
strength of recommendation using GRADE,
the system which is used by the BMJ
(Atkins et al., 2004) (see Table 1). With
score of 4 (high), 3 (moderate), 2 (low) and
1 (very low).

Table 1. Quality and level assessment of articles.

The Quality and Strength
Author/Country Research Design
of Recommendation
(Imran et al, 2015) Pakistan RCT 87 % & 3
(Agarwal et al, 2015) India RCT 78 % & 3
(Jan, Shah, et al, 2012) RCT 80 % & 3
Pakistan
(Kamaratos et al, 2014) Yunani RCT 87 % & 3
(Siavash, et al, 2015) Iran RCT 80 % & 3
(Manalelsayedez et al, 2012) RCT 83 % & 3
Mesir
(Shukrimi, et al, 2008) RCT 77 % & 3
Malaysia
(Abdelatif, et al, 2008) Mesir Prospective pilot 80 % & 3
study
(Moghazy et al., 2010) Mesir Observational 83 % & 3
study
(Henshaw et al., 2014) Prospective 85 % & 3
Australia feasibility study

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8th International Nursing Conference “Education, Practice And Research Development In Nursing”
RESULT
There was 7 of 10 articles discuss
about wound care with honey using RCT
design. 5 of 10 articles was high quality
articles with medium level of
recommendations, 2 articles was medium
quality articles with medium level, and 3
articles used cohort design with a high
quality medium level.
Imran et al (2015) investigated
about the effectiveness of honey in DFU
patients chich is divided in 179 respondents
as honey group and 169 respondents as
control group using normal saline in the
surgical unit of a hospital from February
2006 to February 2010. It is known that
wound completely cured by honey in 136
respondents (75.97%) and 97 (57.39%) with
normal saline. Wounds which is not
significant heals with honey versus normal
saline was 32 (17.87%) versus 53 (31.36%),
(p = 0.001). Healing time: 18.00 (6-120)
days with honey and 29.00 (7-120) days
with normal saline. The conclusion of this
study was honey is effective topical agent in
treatment of DFU.
Agarwal et. Al (2015) compared the
effects of honey with povidone iodine as an
ingredient in the treatment of diabetic foot
ulcers in 36 patients who suffer from type II
Diabetes Mellitus with 2nd degree wounds.
It is known that the average of healing time
with honey: 14.2 days (6-26) days, while in
povidone iodine group: 15.5 days (9-37)
days. Edema, pain and exudate of wounds
also became reduced in honey group. The
results of T-test showed that there was no
significant difference between those two
groups P> 0. 05. It can be concluded that
honey is a alternative which more safe for
the treatment of DFU compared with
povidone iodine.
Jan et al, (2012) investigated about
the effectiveness of honey compared with
povidone iodine in Wagner's Grade I-IV
patients with sample size of 50 patients as
intervention group and 50 others as control
group. The result showed that all patients in
intervention group were completely healed
by 36% and about 14% were amputated,
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8th International Nursing Conference “Education, Practice And Research Development In Nursing”
while in control group using povidone
iodine about 33% of patients were healed
and as about 17% be amputated.
Furthermore, Kamarotos et al (2014) also
investigated the effects of manuka honey-
impregnated dressing (MHID) in healing of
neuropathic diabetic foot ulcers (NDFU)
with sample size of 32 as intervention group
and the control group. The result is known
that wound healing of the MHID group was
31 ± 4 days and the control group was 43 ±
3 days with p value <0.05. There was no
significant difference in the percentage of
wound healing in both groups (97% for
MHID and 90% for the control group).
Research by Siavash Shokri et al
(2015) about the effectiveness of honey (5%
Royal Jelly) in healing of DFU compared
with placebo (gel) in 25 patients who
suffered from type II Diabetes Mellitus. The
average length of wound healing was 23
days for placebo group and 33 days for
groups using Royal Jelly (P = 0.7). The
number of healed wound was 29 of 32
wounds (90.6%) in placebo group and 30
from 32 wounds in group using Royal Jelly
(93.8%) with p value = 0.6. This study
mentioned that 5% topical Royal Jelly
showed no advantages in using placebo for
treatment of DFU.
Manalelsayedez et al (2012)
investigated the effects of honey
(Pedyphar® ointment) compared with
alginate (Fibracol® gel) as a topical
treatment for Type II Wagner DFU. The
result showed that (Pedyphar® ointment)
has 12 ± 3 weeks of healing time while
alginate (Fibracol® gel) has 16 ± 4 weeks
of healing time and there was significant
difference statistically with p value = 0.001.
The conclusion of this study was Honey
(Pedyphar® ointment) more effective than
alginate (Fibracol gel) for the treatment of
type II Wagner DFU.
Shukrimi et al (2008) investigated
the effect of honey compared with povidone
iodine as dressings in the treatment of DFU.
The study was conducted in 30 patients who
suffered from type II Diabetes Mellitus with
Wagner Grade II which is divided into 2
groups: intervention group using honey
dressing and control group using povidine
iodine. Wounds with povidone iodine
dressing has an averageof healing time by
15.4 days (9-36 days). In intervention group
using honey, the average of healing time by
14.4 days (7-26 days). Researcher
concluded that honey could be safe
alternative in the treatment of Wagner
Grade II in patients with DFU.
The next research was research
using cohort design. Abdelatif et al (2008)
investigated the efficacy and safety of
PEDYPHAR (ointment from honey) in
treating patients with DFU. 60 patients with
Diabetes Mellitus were divided into 3
groups based on the stage wound: group 1
(stage I and II), group 2 (stage III) and group
3 (stage IV). The result showed that 96% of
the patients in group 1 and 2 have good
response using PEDYPHAR ointment, and
wound healing occurs. All patients in group
3 healed after surgical excision,
debridement of necrotic tissue, and
conservative treatment using PEDYPHAR
ointment. It can be concluded that
PEDYPHAR ointment may be safe for the
treatment of local DFU.
Moghazy et al (2010) investigated
the effectiveness of honey as topical
treatment for diabetic foot ulcers. The study
was conducted on 30 patients who is
randomly selected. Criteria of the patients
was patient with DFU all degrees of
wounds, all ages and exclude DFU patients
who were amputated. The results showed
that 43% (13 patients) wounds completely
healed for 1-2 months, partially healed in 13
patients (43.3%), patients who experienced
amputation as much as 2 patients (6.7%),
and patients who expeienced skin graft as
much as 2 patients (6.7%). Researcher
mentioned that honey was an effective and
efficient topical alternative for DFU.
Henshaw et al (2014) invetigated the
effectiveness of propolis (honey bee) on
patients with DFU. As many as 24 patients
with Diabetes Mellitus type I and II, all the
degrees of wounds were getting treatment
compared with 84 control patients with
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8th International Nursing Conference “Education, Practice And Research Development In Nursing”
DFU. Wounds were followed up for up to 6
weeks. The results showed that the ulcer
area was reduced with average of 41% in
propolis group compared with 16% in
control group during first week (p < 0.001).
By the third week, ulcer area became 63%
vs 44% (p < 0.05). By the fourth week, ulcer
area became 10% vs 2% (p < 0.001) and by
the seventh week, ulcer area became 19% vs
12% (p < 0.05). it can be concluded that
propolis (honey bee) was a topical treatment
which is effective in treating patients with
DFU.
DISCUSSION
Honey has the effect of antibiotics,
antioxidants, anti-inflammatory, auto
debridement, stimulation of growth factors
and good osmolarity in wound healing
(Chapman, 2009). Furthermore, all of the 10
articles which has been reviewed by
researcher contain the benefits of honey in
the treatment of diabetic foot ulcers.
According to (Kateel, Adhikari, Augustine,
and Ullal, 2016) honey dressing is safer to
used in the treatment of diabetic foot ulcers
because honey accelerates wound healing,
has the effect of anti-inflammatory and anti-
bacterial, and reduce the number of
amputations. It is also found in the article
discussed by (Tian et al., 2014) which said
that the total time of treatment, the average
time of cleaning the ulcer, the number of
bacteria, and healing the wound area using
honey was better.
Total of 7 articles using RCT design
concluded that wound care with honey was
more effective in treating DFU although
there was some articles that showed no
significant effects. But honey showed its
effect of healing faster than the others. The
last three observational studies was very
strong research with medium level
recommendations. Those studies concluded
that honey is more effective in wound care
of DFU for all degrees of wounds, have
anti-inflammatory and anti-bacterial
characteristic, accelerate granulation,
autolysis, and cost effective (Moghazy et
al., 2010). This is consistent with research
by (Tsang et al., 2015) which mentioned
that honey has many benefits such as anti-
inflammatory, anti-cancer, anti-ulcer, anti-
viral, anti-fungal, vasodilators, and many
more. By looking at a variety of evidence
that already exists and the benefits of honey,
it can be said that honey was a highly
effective topical to heal diabetic foot
wounds (DFU).
CONCLUSION AND SUGGESTION
Several articles have been reviewed
and it is known that honey is a good
alternative choice in wound care of DFU.
Meanwhile, to conclude that honey is one of
the best alternatives in wound care requires
a lot of randomized clinical study which
compares honey with a variety of existing
topical agents.
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