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JBUR-4991; No.

of Pages 8

burns xxx (2016) xxx–xxx

Available online at www.sciencedirect.com

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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 . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
Acknowledgements . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000
References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 000

that the search was comprehensive, the reference lists of the


1. Introduction retrieved articles and any identified review articles were
reviewed. In addition, the corresponding authors of identified
Burn injuries are common. The definition of burns by the studies were contacted, and experts working in the field of burn
World Health Organization [1] is ‘‘an injury to the skin or other therapy or honey, were asked for further studies. RCTs
organic tissue primarily caused by heat, radiation, radioactiv- involving silver compared with honey for burn wound healing
ity, electricity, friction or contact with chemicals’’. The were included. No restriction on the language, date, and
severity of burn injuries depends on the depth of the wound publication type of the studies was applied. The relevant data
injury and the extent of the body area affected. As a result of were extracted by two reviewers and methodological quality
burn injuries, the skin loses its protective function against was assessed using the Cochrane Criteria for Risk of Bias
microorganisms leading to a high risk of infection. Burn assessment [19]. Any disagreements between the two reviewers
wounds are also susceptible to infection because their moist were resolved through discussion.
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 3. Data analysis
medical costs [3], impairment in work and quality of life and
can lead to social rejection due to disfigurement [1]. The Trials were only included if they used time for burn healing or
prevention of infection, therefore, is an important factor in the infection rate as primary outcomes. Measures such as pain
acceleration of healing and reduction of morbidity [1]. and adverse events were the secondary outcomes. The
Recently, topical dressings containing honey as well as silver outcome measure used for statistical pooling was burn healing
sulfadiazine (SSD) have re-emerged as a treatment option for reported either as dichotomous or continuous outcomes. For
burn wound management [4]. Honey is postulated to facilitate dichotomous outcomes, relative risk (RR) was calculated and
wound healing by its chemical debridement and anti-inflam- the results were reported as RR with 95% confidence intervals
matory action [5], and its ability to create a viscous barrier on (CI) while for healing time, results were collected on the
the wound surface thus preventing the invasion of micro- reported mean difference (MD), the weighted mean difference
organisms [5–8]. Meanwhile, SSD may be considered as the gold (WMD), or standardized mean difference (SMD) with 95% CI as
standard for topical burn treatment [9]. In contrast to honey, appropriate between the silver and honey groups. In some
silver-containing dressings are capable of absorbing the burn studies where data required for meta-analysis was missing,
exudates and releasing silver which has been recognized as an attempts were made to contact the original authors for
effective antimicrobial agent against a broad range of bacteria, detailed information. If standard deviation could not be
yeast, and viruses [3,10]. However, recent findings have shown obtained, equal variance and normal distribution of the data
that topical silver delays rather than promotes wound healing were assumed, and standard deviations based on the p-value
and is associated with potentially severe adverse effects [11–13]. provided in the articles were calculated.
Several systematic reviews have examined the effective- Statistical heterogeneity was analyzed using the Index, I2
ness of both silver and honey for acute and chronic wounds test as recommended by The Cochrane Collaboration. If the I2
including burn injuries [14–17]. However, none of these statistic was deemed high (over 75%) we explored the
reviews specifically compared the efficacy of honey versus heterogeneity [20].
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. 4. Results

The flow of searches, and number of trials identified and


2. Materials and methods included in this study are shown in Fig. 1. Of the 5150 records
identified, 17 full text articles were assessed and 7 studies were
The following databases were searched; MEDLINE (1966–2014), excluded for reasons as stated in Fig. 1. Only ten trials met the
Cumulative Index of Nursing & Allied Health Literature; CINAHL inclusion criteria and of these, nine trials provided quantita-
(1982–2014), Cochrane Database of Systematic Reviews (1996– tive data and were therefore included in the quantitative
2014), Cochrane Central Register of Controlled Trials (1991– analysis.
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 5. Description of studies
(RCTs) in all databases as described elsewhere [18]. For the
search strategy, the Medical Subject Headings ‘‘Silver’’ and A total of ten trials were included with a total of 717 patients
‘‘Honey’’ AND ‘‘burn’’ OR ‘‘burn wound’’ were used. To ensure with a variety of burn wounds (Table 1). Four trials [8,21–23]

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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Fig. 1 – Study flow diagram of result of searches, studies identified and included in this review.

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

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
4

JBUR-4991; No. of Pages 8


A systematic review of randomized controlled trials. Burns (2016), http://dx.doi.org/10.1016/j.burns.2016.07.004
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:

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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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.
Fig. 2 – Risk of bias summary. 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
7.2. Wounds healed (proportion) compared to non-silver dressings, silver was shown to worsen
healing time. However, silver is still used as a comparator or
Only three trials [24,28,29] provided data for the proportion of control in many burn trials because it is considered as the gold
patients with completely healed wounds. Pooling of data standard in the treatment of burn wounds [9,35,36]. Thus, it
(Fig. 4) shows that there is a statistically significant difference seems that when honey is compared to silver, the effect of
between the two groups in the proportion of patients with honey on wound healing may be amplified rather than honey
wounds healed favoring the honey group (RR 2.13; 95% CI 1.61– being truly effective.
2.80). It is difficult to judge the quality of the evidence as the
majority of the domains in the risk of bias assessment were
7.3. Number of infected wounds rendered sterile inadequately described. Additionally, about half of the
included studies were open trials. Although blinding of
Seven trials reported the number of infected wounds rendered participants and care providers was difficult, the trial
sterile [8,21–23,25,28,29]. As shown in Fig. 5, the pooled results investigators could have blinded the outcome assessors to
for the three subgroups (superficial thickness, partial thick- reduce the risk of outcome bias. If information on group
ness, and superficial and partial thickness wounds) shows a assignment is not concealed from participants, their

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
JBUR-4991; No. of Pages 8

6 burns xxx (2016) xxx–xxx

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

burns xxx (2016) xxx–xxx 7

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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