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of Pages 8

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Available online at www.sciencedirect.com

ScienceDirect

journal homepage: www.elsevier.com/locate/burns

Review

The effects of honey compared to silver

sulfadiazine for the treatment of burns:
A systematic review of randomized controlled trials

Zoriah Aziz *, Bassam Abdul Rasool Hassan

Department of Pharmacy, Faculty of Medicine, University of Malaya, 50603, Kuala Lumpur, Malaysia

article info abstract

Article history: Evidence from animal studies and trials suggests that honey may accelerate wound healing.
Accepted 14 July 2016 The objective of this review was to assess the effects of honey compared with silver
dressings on the healing of burn wounds. Relevant databases for randomized controlled
Keywords: trials (RCTs) of honey compared with silver sulfadiazine (SSD) were searched. The quality of
Honey the selected trials was assessed using the Cochrane Risk of Bias Assessment Tool. The
Silver sulfadiazine primary endpoints considered were wound healing time and the number of infected
Dressing wounds rendered sterile. Nine RCTs met the inclusion criteria. Based on moderate quality
Burn evidence there was a statistically significant difference between the two groups, favoring
Healing time honey in healing time (MD 5.76 days, 95% CI 8.14 to 3.39) and the proportions of infected
Meta-analysis wounds rendered sterile (RR 2.59; 95% CI 1.58–2.88). The available evidence suggests that
honey dressings promote better wound healing than silver sulfadiazine for burns.
# 2016 Elsevier Ltd and ISBI. All rights reserved.

Contents

1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
2. Materials and methods . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
3. Data analysis . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
4. Results . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
5. Description of studies . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
6. Risk of bias assessment in included trials . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7. Effects of intervention . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7.1. Complete wound healing time . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7.2. Wounds healed (proportion) . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7.3. Number of infected wounds rendered sterile . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7.4. Pain . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
7.5. Adverse events . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
8. Discussion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000

* Corresponding author: Tel.: +603 79674909; fax: +603 79674964.

E-mail address: zoriah@um.edu.my (Z. Aziz).
http://dx.doi.org/10.1016/j.burns.2016.07.004
0305-4179/# 2016 Elsevier Ltd and ISBI. All rights reserved.

Please cite this article in press as: Aziz Z, Abdul Rasool Hassan B. The effects of honey compared to silver sulfadiazine for the treatment of burns:
A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
JBUR-4991; No. of Pages 8
2 burns xxx (2016) xxx–xxx
9. Conclusion . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . .
1. Introduction
Burn injuries are common. The definition of burns by the
World Health Organization [1] is ‘‘an injury to the skin or other
organic tissue primarily caused by heat, radiation, radioactiv-
ity, electricity, friction or contact with chemicals’’. The
severity of burn injuries depends on the depth of the wound
injury and the extent of the body area affected. As a result of
burn injuries, the skin loses its protective function against
microorganisms leading to a high risk of infection. Burn
wounds are also susceptible to infection because their moist
environment provides an ideal situation for bacteria to
multiply [2]. Infection by microorganisms is a major cause
of morbidity associated with extended hospital stay and high
medical costs [3], impairment in work and quality of life and
can lead to social rejection due to disfigurement [1]. The
prevention of infection, therefore, is an important factor in the
acceleration of healing and reduction of morbidity [1].
Recently, topical dressings containing honey as well as silver
sulfadiazine (SSD) have re-emerged as a treatment option for
burn wound management [4]. Honey is postulated to facilitate
wound healing by its chemical debridement and anti-inflam-
matory action [5], and its ability to create a viscous barrier on
the wound surface thus preventing the invasion of micro-
organisms [5–8]. Meanwhile, SSD may be considered as the gold
standard for topical burn treatment [9]. In contrast to honey,
silver-containing dressings are capable of absorbing the burn
exudates and releasing silver which has been recognized as an
effective antimicrobial agent against a broad range of bacteria,
yeast, and viruses [3,10]. However, recent findings have shown
that topical silver delays rather than promotes wound healing
and is associated with potentially severe adverse effects [11–13].
Several systematic reviews have examined the effective-
ness of both silver and honey for acute and chronic wounds
including burn injuries [14–17]. However, none of these
reviews specifically compared the efficacy of honey versus
SSD in burn wounds. Thus, the aim of this systematic review
was to determine the efficacy of honey compared to SSD in
burn wound healing.
2. Materials and methods
The following databases were searched; MEDLINE (1966–2014),
Cumulative Index of Nursing & Allied Health Literature; CINAHL
(1982–2014), Cochrane Database of Systematic Reviews (1996–
2014), Cochrane Central Register of Controlled Trials (1991–
2014), and Database of Abstract of Reviews of Effects; DARE
(2001–2014). The search of MEDLINE was limited to humans and
a filter was applied to identify Randomized Controlled Trials
(RCTs) in all databases as described elsewhere [18]. For the
search strategy, the Medical Subject Headings ‘‘Silver’’ and
‘‘Honey’’ AND ‘‘burn’’ OR ‘‘burn wound’’ were used. To ensure
Please cite this article in press as: Aziz Z, Abdul Rasool Hassan B. The effects of honey compared to silver sulfadiazine for the treatment of burns:
A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
000
000
000
that the search was comprehensive, the reference lists of the
retrieved articles and any identified review articles were
reviewed. In addition, the corresponding authors of identified
studies were contacted, and experts working in the field of burn
therapy or honey, were asked for further studies. RCTs
involving silver compared with honey for burn wound healing
were included. No restriction on the language, date, and
publication type of the studies was applied. The relevant data
were extracted by two reviewers and methodological quality
was assessed using the Cochrane Criteria for Risk of Bias
assessment [19]. Any disagreements between the two reviewers
were resolved through discussion.
3. Data analysis
Trials were only included if they used time for burn healing or
infection rate as primary outcomes. Measures such as pain
and adverse events were the secondary outcomes. The
outcome measure used for statistical pooling was burn healing
reported either as dichotomous or continuous outcomes. For
dichotomous outcomes, relative risk (RR) was calculated and
the results were reported as RR with 95% confidence intervals
(CI) while for healing time, results were collected on the
reported mean difference (MD), the weighted mean difference
(WMD), or standardized mean difference (SMD) with 95% CI as
appropriate between the silver and honey groups. In some
studies where data required for meta-analysis was missing,
attempts were made to contact the original authors for
detailed information. If standard deviation could not be
obtained, equal variance and normal distribution of the data
were assumed, and standard deviations based on the p-value
provided in the articles were calculated.
Statistical heterogeneity was analyzed using the Index, I2
test as recommended by The Cochrane Collaboration. If the I2
statistic was deemed high (over 75%) we explored the
heterogeneity [20].
4. Results
The flow of searches, and number of trials identified and
included in this study are shown in Fig. 1. Of the 5150 records
identified, 17 full text articles were assessed and 7 studies were
excluded for reasons as stated in Fig. 1. Only ten trials met the
inclusion criteria and of these, nine trials provided quantita-
tive data and were therefore included in the quantitative
analysis.
5. Description of studies
A total of ten trials were included with a total of 717 patients
with a variety of burn wounds (Table 1). Four trials [8,21–23]
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Fig. 1 – Study flow diagram of result of searches, studies identified and included in this review.

included patients with superficial thickness wounds; three
trials [24–26] included patients with partial thickness wounds,
while the other three trials [27–29] included patients with
superficial thickness and partial thickness wounds.
Undiluted honey was used in all of the trials except one [23].
Topical honey + dressings were used in all trials; seven trials
compared it with topical silver agents + dressings [23–29]
while three trials compared it with silver-containing dressings
[8,21,22].
Primary outcome measures such as time taken to complete
wound healing and number of wounds rendered sterile were
reported in most of the studies. Secondary outcome measures
such as pain were only reported in two trials [25,27] and the
adverse effect of interventions were not reported in any of the
studies.
6. Risk of bias assessment in included trials
The risk of bias of the included studies is summarized in Fig. 2.
The majority of the trials had unclear risk of bias for sequence
generation, concealment of allocation, and blinding of
participants and outcome assessor. However one trial [25]
was judged to have high risk of bias for randomization as the
trial used a consecutive sampling method which was a type
of non-probability sampling [30] that could cause selection
bias. There was no loss to follow up in any of the included
studies.
Trials were determined as having low risk of bias for the
domain ‘‘selective outcome reporting’’ when outcomes mea-
sures specified in the methods section were also reported in the
results. Except for two trials, [22,26] all other trials were judged
to have low risk of bias. For other potential bias, the focus was
on baseline comparability between honey and silver treated
groups. All the trials reported comparable baseline character-
istics between the intervention and control groups.
7. Effects of intervention
Out of 10 included trials; quantitative data were only available
for 9 trials. The results were based on outcome measures,
which were commonly reported among the included trials.
These outcomes were also presented in previous systematic
reviews looking at different interventions for burn wounds.
7.1. Complete wound healing time
Results for only four trials involving superficial and partial
thickness burns were suitable for pooling [8,21–23]. The pooled
effect using the random-effect model (I2 = 93%) showed a
statistically significant effect favoring honey for superficial
thickness wounds (MD 4.62; 95% CI 7.37 to 1.88) (Fig. 3).
Two other trials [26,27] just reported that the duration of
wound healing was shorter in the group treated with honey
compared to the group treated with silver.

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A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
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Table 1 – Characteristics of RCT included in this study.

Study (Country) Participants Age in years Intervention: Control: Duration Outcomes reported
(mean (SD)/range) (No. of subjects) (No. of subjects) of study
Baghel et al. [28] (India) 78 patients with first and H: 34.5 (NR) Honey-added (pure, SSD cream 2 months Wound healing time, time
second degree burns unprocessed, and (n = 41) taken to render wounds
C: 28.5 (NR) undiluted) dressings sterile, proportion of wound
(n = 37) healed
Sami et al. [25] (Pakistan) 50 patients with partial 1.5–50 Pure, unprocessed, and 1% SSD cream 2 months Time required for healing,
thickness thermal burns undiluted topical honey (n = 25) number of infected wounds
(n = 25) rendered sterile, complete
pain relief, cost per dressing
per % burn
Bangroo et al. [23] (India) 64 patients with superficial Less than Honey SSD Until wounds Wound healing time, time
thermal burns 12 years old (n = 32) (n = 32) healed taken to sterilize the wound
Shah et al. [29] (Pakistan) 84 Patients with first and 25.95 (16.7) Pure and undiluted honey SSD cream 2 months Duration of healing, time
second degree burns (n = 42) (n = 42) taken to achieve sterilization

burns xxx (2016) xxx–xxx

of wound
Mashhood et al. 50 patients with superficial 27.4 (NR) Honey-added (pure, 1% SSD cream Until wound Wound healing time, pain,
[27] (Pakistan) and partial thickness burns unprocessed, and (n = 25) healed time taken by the wound to
undiluted) dressings get sterilized, proportion of
(n = 25) wound healed
Mujalde et al. [26] (India) 110 patients with partial 10–50 Undiluted pure honey with SSD cream with Until wound Wound healing time, time
thickness burns less than sterile gauge, cotton pad, sterile gauge, epithelialized taken to sterilize the wound
50% roller bandage cotton pad,
of total body surface area (n = 55) roller bandage
(n = 55)
Okeniyi et al. [24] (Nigeria) 27 children with partial 5.5 (3.4) Crude undiluted honey SSD (Dermazine1) 21 days Clinical condition of burn
thickness burns dressing dressing sites at day 3,7, and 21,
(n = 15) (n = 12) duration of hospital stay,
cost of treatment
Subrahmanyam [8] (India) 104 patients with superficial 1–65 Honey (pure, unprocessed, Silver sulfadiazine 2 months Wound healing time
thermal burns undiluted) dressing impregnated gauze
(n = 52) (n = 52)
Subrahmanyam [21] (India) 50 patients with superficial H: 25.2 (NR) Honey-added (pure, SSD impregnated 1 month Wound healing time, wound
thermal burns C: 26.4 (NR) unprocessed) dressings gauze infection (number of cases),
(n = 25) (n = 25) proportion of wound healed
Subrahmanyam et al. 100 patients with superficial H: 26.5 (1.0) Honey-added (pure, SSD impregnated Until wound Wound healing time, time
[22] (India) burns C: 25.2 (2.0) unprocessed) dressings gauze healed taken by the wound to get
(n = 50) (n = 50) sterilized, proportion of
wound healed, subjective
relief of pain
Note: n = number of participants; SSD = silver sulfadiazine, NR = not reported, H = Honey, C = Control.
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Fig. 2 – Risk of bias summary.
7.2. Wounds healed (proportion)
Only three trials [24,28,29] provided data for the proportion of
patients with completely healed wounds. Pooling of data
(Fig. 4) shows that there is a statistically significant difference
between the two groups in the proportion of patients with
wounds healed favoring the honey group (RR 2.13; 95% CI 1.61–
2.80).
7.3. Number of infected wounds rendered sterile
Seven trials reported the number of infected wounds rendered
sterile [8,21–23,25,28,29]. As shown in Fig. 5, the pooled results
for the three subgroups (superficial thickness, partial thick-
ness, and superficial and partial thickness wounds) shows a
Fig. 3 – Comparison: Honey versus silver; Outcome: Complete wound healing time (days).
Please cite this article in press as: Aziz Z, Abdul Rasool Hassan B. The effects of honey compared to silver sulfadiazine for the treatment of burns:
A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
5
statistically significant beneficial effect favoring honey (RR
9.08; 95% CI 1.69–48.81).
7.4. Pain
Two trials [25,27] reported the proportion of patients with
complete pain relief at 3 weeks and the pooled analysis
showed that there was no significant difference between the
two groups (RR 1.00; 95% CI 0.41–2.44).
7.5. Adverse events
None of the studies reported adverse events.
8. Discussion
Based on the evidence, for superficial or partial thickness
wounds, honey was found to have statistically significant
beneficial effects compared to SSD for the outcomes time to
complete wound healing, proportion of wounds completely
healed, and proportion of infected wounds rendered sterile.
However, it should be noted that the heterogeneity among the
included studies for the meta-analysis of complete wound
healing time and number of infected wounds rendered sterile
was high (more than 90%) due to variations in the age of
included participants, duration of follow up, and the types of
outcomes reported.
Data from animal studies and human trials suggests that
silver delays wound healing as it is toxic to regenerating
keratinocytes [31–35]. Additionally, in a systematic review
published in 2012, Aziz et al. [11] reported that when silver was
compared to non-silver dressings, silver was shown to worsen
healing time. However, silver is still used as a comparator or
control in many burn trials because it is considered as the gold
standard in the treatment of burn wounds [9,35,36]. Thus, it
seems that when honey is compared to silver, the effect of
honey on wound healing may be amplified rather than honey
being truly effective.
It is difficult to judge the quality of the evidence as the
majority of the domains in the risk of bias assessment were
inadequately described. Additionally, about half of the
included studies were open trials. Although blinding of
participants and care providers was difficult, the trial
investigators could have blinded the outcome assessors to
reduce the risk of outcome bias. If information on group
assignment is not concealed from participants, their
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Fig. 4 – Comparison: Honey versus silver; Outcome: Wound healed (proportion).

Fig. 5 – Comparison: Honey versus silver; Outcome: Number of infected wounds rendered sterile.

Please cite this article in press as: Aziz Z, Abdul Rasool Hassan B. The effects of honey compared to silver sulfadiazine for the treatment of burns:
A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
JBUR-4991; No. of Pages 8
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responses to the intervention are most likely to be affected
[37]. Likewise, investigators who are not blinded can affect the
participants’ attitude towards the intervention received, as
well as the participants’ compliance throughout the length of
study [38]. Another limitation of this review is that the
outcome assessment for wound healing is not consistent
among studies as most of the trial authors did not explicitly
state the definition of wound healing and how it was
measured.
In the light of all these limitations, the findings of this
review should be interpreted with caution. The results of this
review are in agreement with other reviews examining
evidence of effectiveness of honey for wound healing [16,17]
where the quality of evidence in the included trials limits the
drawing of a firm conclusion regarding the beneficial effects of
honey for burn wound management.
9. Conclusion
Despite a positive finding favoring honey when compared to
silver, the scarcity of high quality evidence to justify routine
use of honey for burn wound healing in clinical practice is
highlighted in this review. Authors of future trials should use
common and clinically relevant end-points to assess the
effectiveness of honey, and to use the Consolidated Standards
of Reporting Trial (CONSORT) statement to improve the
quality of reporting of trials.
Given the evidence that silver delays re-epithelialization,
its use as a control or comparator should also be reassessed in
future trials as any intervention would almost always be found
more effective than silver.
Acknowledgements
We would like to thank Chong Nyuk Jet and Wei Ling Tang for
their assistance in retrieving the articles and extracting data.
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