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diabetes research and clinical practice 89 (2010) 276–281

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Diabetes Research
and Clinical Practice
jou rna l hom ep ag e: w ww.e lse v ier .com/ loca te /d iab res

The clinical and cost effectiveness of bee honey dressing in


the treatment of diabetic foot ulcers

A.M. Moghazy a,*, M.E. Shams a, O.A. Adly a, A.H. Abbas a, M.A. El-Badawy a,
D.M. Elsakka b, S.A. Hassan a, W.S. Abdelmohsen a, O.S. Ali a, B.A. Mohamed a
a
Faculty of Medicine, Suez Canal University, Ismailia, Egypt
b
Faculty of Medicine, Menofia University, Shebeen El-Koom, Egypt

article info abstract

Article history: Honey is known, since antiquity, as an effective wound dressing. Emergence of resistant
Received 25 February 2010 strains and the financial burden of modern dressings, have revived honey as cost-effective
Received in revised form dressing particularly in developing countries. Its suitability for all stages of wound healing
7 May 2010 suggests its clinical effectiveness in diabetic foot wound infections.
Accepted 20 May 2010 Thirty infected diabetic foot wounds were randomly selected from patients presenting to
Published on line 19 June 2010 Surgery Department, Suez Canal University Hospital, Ismailia, Egypt. Honey dressing was
applied to wounds for 3 months till healing, grafting or failure of treatment. Changes in
Keywords: grade and stage of wounds, using University of Texas Diabetic Wound Classification, as well
Honey as surface area were recorded weekly. Bacterial load was determined before and after honey
Diabetic foot infection dressing.
Clinical effectiveness Complete healing was significantly achieved in 43.3% of ulcers. Decrease in size and
Ideal dressing healthy granulation was significantly observed in another 43.3% of patients. Bacterial load of
Cost effectiveness all ulcers was significantly reduced after the first week of honey dressing. Failure of
treatment was observed in 6.7% of ulcers.
This study proves that commercial clover honey is a clinical and cost-effective dressing for
diabetic wound in developing countries. It is omnipresence and concordance with cultural
beliefs makes it a typical environmentally based method for treating these conditions.
# 2010 Elsevier Ireland Ltd. All rights reserved.

1. Introduction Despite recent advances in antimicrobial therapy, diabetic


foot infections are still a serious problem. Although topical, as
Diabetic foot ulcers are major cause of morbidity and disability well as systemic, antibiotics and agents have been used, solely
in diabetic patients. They frequently lead to lower extremity and in combination, to eradicate this resistant infection, it
amputations especially when associated with neuropathy persisted. Moreover, these agents had lead to the emergence,
and/or ischemia [1,2]. and subsequent rapid overgrowth, of resistant bacterial
On the national level, foot ulceration is common; it affects strains, drug side-effects and organ specific toxicity [5–7].
6.9% of diabetics during their life time [3]. Moreover, ulceration Medicinal properties of honey have been recognized since
is the most common cause of hospitalization and precedes antiquity [8]. It was used as a wound dressing to treat infected
80% of lower limb amputations [4]. wounds and promote healing. Modern studies revealed its

* Corresponding author at: Department of Surgery, Faculty of Medicine, Suez Canal University, Ismailia, Egypt. Tel.: +20 (0)10 5730231;
fax: +20 (0)64 3208543.
E-mail addresses: moghazy@yahoo.com, a.moghazy@scuegypt.edu.eg (A.M. Moghazy).
0168-8227/$ – see front matter # 2010 Elsevier Ireland Ltd. All rights reserved.
doi:10.1016/j.diabres.2010.05.021
diabetes research and clinical practice 89 (2010) 276–281 277

effectiveness against antibiotic-resistant strains of bacteria; it from the wound for culture and sensitivity. If the wound was
prevents bacterial growth even when wounds are heavily initially showing signs of invading infection, a combination of
infected [9–11]. Even when it was ineffective, it never resulted ciprofloxacin and mitronidazole was started for 5 days. If
in the emergence of resistant strains [12]. The antimicrobial infection was to appear during the study, antibiotic therapy
activity of bee honey has been attributed to several properties, was to be given according to the result of the last culture.
including its osmotic effect, naturally low pH, and the As we are convinced that processing of honey might alter
production of hydrogen peroxide [13–15]. It therefore seems its effectiveness (altering the ration of its components), pure
time to revive honey as dressing for these resistant wounds. raw untreated commercial honey was used in this work (no
additives, pasteurization or manipulations). To assure highest
quality and purity of honey, it was supplied by the Firm of
2. Aim of the work Faculty of Agriculture, Alexandria University. Honey was
applied the form of impregnated gauze.
This study was conducted to investigate the value of honey as
topical treatment for diabetic foot ulcers. In addition, analysis 4.1. Preparation of honey impregnated gauze
of wound factors and criteria of patient that affect the
outcome of honey dressing was done to optimize its use. Medium-pored non-sterile gauze was used in this study.
According to the surface area of the wound, the length of the
gauze piece was determined (it should cover the whole wound
3. Patients and hang over the edges in two layers for a single piece). The
number of the pieces depended upon the depth of the wound
Thirty patients complaining of diabetic foot ulcers presenting (the gauze should fill the whole depth of the wound to above
to the Surgery Department, Suez Canal University Hospital, the surrounding skin level).
Ismailia, Egypt in the period between March and September Prior to the dressing session, the gauze length was cut (with
2007 were submitted to this study. about 10 cm more than the desired size), and submerged in a
Patients of all ages and both sexes were included in this deep container to be folded over itself smoothly in multiple
study. All patients with diabetic foot ulcers, regardless of their layers. The other edge was left to hang over the edge of the
depths, areas or presence of infection were included in the container. The gauze was left to be saturated with honey
present work. Patient selection was done by randomly allocat- during the wound bed preparation. Excess honey was
ing patients presenting to Surgery Department, either through removed, particularly in highly oozing wounds, by passing
outpatient or consultation from inpatient till reaching the the gauze between the firmly opposed middle and ring fingers.
sample size (30 patients). This was achieved after 6 months. Patients and their relatives were taught the method of
The exclusion criteria were pending amputation (due to preparing and applying the honey impregnated gauze in the
sever vascular compromise and/or toxemia) and immuno- initial visit or during hospitalization.
compromised patients (e.g. chemotherapy or steroid therapy).
As all the patients who attend the Surgery Clinic are mostly 4.2. Dressing technique
of resistant wound type, i.e. with at least 3 months history of
cessation of progression or worsening of the wound, there was Patients were treated on outpatient clinic except when there
no need to have control group as the patients themselves were was an indication for admission (bad glucose control, need for
considered control before starting honey dressing. In addition, surgical debridement, vascular insufficiency, . . ., etc.). As soon
the same regimen that was followed in the previous period as the indication of hospitalization was overcome, patients
was the same applied to the study except for using honey as were referred to outpatient clinic for follow-up.
topical dressing to standardize all the factors implemented in The wound was meticulously debrided (sometimes under
wound management in both periods. anesthesia) and thoroughly washed using normal saline (no
antiseptic). Heavily infected wounds were rinsed with warm
tap water after debridement. After drying the wound, honey
4. Methods impregnated gauze was applied. The gauze was held from the
non-impregnated part (removed after application by scissors).
The surface area of all wounds was used to assess the initial size Fluffy dressing was applied over the gauze and kept in place by
and evaluate the progress. For irregular wounds, surface area bandage.
was calculated by multiplying the two largest dimensions. If the Frequency of dressing depended upon the amount of
wound was roughly circular, quadrangular or triangular, the exudates; whenever the dressing is soaked, it should be
surface area was calculated according to the geometrical rules. changed by the same technique. Once single daily dressing
In addition, for deep wounds (reaching the subcutaneous was reached, provided all the other parameters were accepted,
tissue), University of Texas Diabetic Wound Classification [16] the patient was discharged and followed up in the outpatient
was used to assess the grade and stage of the ulcers. clinic on weekly basis.
At the initial visit, the patient was assessed through All patients received vitamin B complex for life. Health
detailed history and thorough clinical examination. Peripheral education was provided to all patients. The education program
neuropathy and vascular sufficiency were judged clinically emphasized on the importance of: follow-up in the clinic, foot
through sensory, motor and trophic changes. Following the hygiene, nail care, proper footwear, nutritional regimen and
diabetic foot regimen management, bacterial swab was taken management of newly healed foot ulcer.
278 diabetes research and clinical practice 89 (2010) 276–281

For follow-up, monthly wound measurements, photos and Table 1 – The change of the ulcer size throughout the
culture were obtained (in addition to the routine follow-up of whole period of follow-up.
the laboratory and other medical investigations of the diabetic Follow-up Range (cm2) N = 30 100% Chi-square
patient). period

At initial visit 1–5 8 26.8 0.0002**


6–10 13 43.3
5. Results 11–15 1 3.3
16–20 1 3.3
Table 1 demonstrates demographic data of patients partici- 21–105 7 23.3
After 1 month 0 4 13.3
pating in this study. The majority of our patients (46.7%) were
1–5 9 30
in their sixth decade of their life with mean age of 52.3 years.
6–10 8 26.8
Two thirds of our patients were males. All the smokers in this 11–15 2 6.7
study (56.7%) were males. 16–20 1 3.3
Table 2 shows the diabetic profile of patients participating 21–105 4 13.3
in the study. Twenty-eight patients (93.3%) were type II. After 2 months 0 (4 + 4a) 26.8 <0.0001**
Twenty patients (66.7%) were diabetics for more than 10 years. 1–5 10 33.3
6–10 4 13.3
Percentage of control in patients on insulin therapy (64.7%)
11–15 1 3.3
was less than those on oral hypoglycemic drugs (92.3%).
16–20 1 3.3
Regarding the peripheral neuropathy (PN), only 9 patients 21–75 3 10
(30%) had no PN. After 3 months 0 (5 + 4a + 4a) 43.3 <0.0001**
In this study, only 6 patients (20%) had no vascular disease. 1–5 10 33.3
Table 3 shows the change of the ulcer size throughout the 6–10 0 0
whole period of follow-up. The ulcer size decreased, with 11–15 1 3.3
16–20 1 3.3
highly significant statistic rates, in 28 patients (93.3%); the
21–24 1 3.3
remaining 2 patients (6.7%) were candidates for amputation.
Table 4 demonstrates the progression in grade and stage of a
Number of previous resurfaced ulcer.
**
the wounds throughout the whole period of the study. Significance P < 0.01.
Improvement, in grade and stage (G&S), of ulcers was
significant along the whole period of study. patient (3.3%) showing persistence of inflammatory signs (2
At the initial visit, the highest frequency of G&S was 1-b in patients were subjected to amputation).
20 patients (66.7%). The lowest frequency was 2-d in 1 patient Starting from the second month, no patient showed signs
(3.3%). After the first month, the highest frequency was 2-a in of inflammation in the ulcer.
18 patients (60%). By the end of second month, the highest Table 6 demonstrates the presence and nature of exudates
frequency was 1-a in 13 patients (46.7%). The lowest frequency in the wound. There was significant improve in the amount
was in 6 patients (20%) in G&S of 2-a. and nature of discharge throughout the whole study period.
At the end of the study, the highest frequency was found in The highest frequency of ulcer exudates was foul and
12 patients (40%) in G&S of 1-a. The lowest was in 1 patient profuse in 23 ulcers (76.7% of the studied group) by the initial
(3.3%) in G&S of 2-a. assessment.
Table 5 shows the presence of inflammation signs in the After 1 month, the highest frequency was serosanguinous
wound during the period of the study. All ulcers showed signs moderate exudate in 22 ulcers (73.3%).
of inflammation in initial assessment. After 1 month, 27 In the second month, there were 11 ulcers (36.7%) had
patients (90%) showed significant improvement with only 1 scanty serous exudates.

Table 2 – The progression in grade and stage of the wounds throughout the whole period of the study.
Grade and stage Initial visit First month Second month Third month

N % N % N % N %
a a a
0-a 0 0 4 13.3 4 +4 26.8 4 +4 +5 43.3
1-a 0 0 4 13.3 14 46.7 12 40
2-a 0 0 18 60 6 20 1 3.3
1-b 20 66.7 1 3.3 0 0 0 0
2-b 7 23.3 0 0 0 0 0 0
2-c 0 0 1 3.3 0 0 0 0
2-d 1 3.3 0 0 0 0 0 0
3-d 2 6.7 0 0 0 0 0 0

Chi-square <0.0001* 0.01* <0.0001*

a
Number of cases healed from previous period and not included.
*
Significance P < 0.01.
diabetes research and clinical practice 89 (2010) 276–281 279

Table 3 – The presence of inflammation signs in the Table 6 – The presence and nature of exudates in the
wound during the period of the study. wound.
Period Inflammatory P-value Discharge Initial First Second Third
response nature visit month month month

N = 30 100% Not characteristic


*
N 0 0 11 12
Baseline data 30 100 <0.001
% 0 0 36.7 40
After first month 1a 3.3
After second month 0 0 Foul/purulent
After third month 0 0 N 23 0 0 0
% 76.7 0 0 0
a
Two patients have had amputation within the first month.
* Serosanguinous
Significance P < 0.01.
N 7 24 8 0
% 23.3 80 26.8 0

Chi-square <0.001* <0.001* <0.001*


Table 4 – The nature of exudates in the wound.
*
Discharge Initial First Second Third Significance P < 0.01.
nature visit month month month

Not characteristic
Table 7 – The frequency of isolated microorganisms from
N 0 0 11 12
the studied group before and after honey dressing.
% 0 0 36.7 40
Microorganisms Before After
Foul/purulent
N 23 0 0 0 N = 30 100% N = 30 100%
% 76.7 0 0 0
No 0 0 0 0
Serosanguinous Staphylococcus aureus 12 40 0 0
N 7 24 8 0 Staphylococcus epidermidis 6 20 28 93.3
% 23.3 80 26.8 0 Echerichia coli 5 16.7 0 0
Chi-square <0.001* <0.001* <0.001* Proteous 3 10 0 0
Klebsiella spp. 2 6.7 0 0
*
Significance P < 0.01. Provedentia 1 3.3 0 0
Pseudomonas aerugenosa 1 3.3 2 6.7

By the end of the study, all ulcers had serous very scanty
exudate. wounds) or showing healthy granulation and surface area
The type and amount of exudate varied significantly every reduction (13 patients) by the end of the study.
month throughout the whole period of the study. Amputation was the outcome in two cases (6.7%). Graft was
Table 7 shows the percentage differentiation of micro- done in one case (3.35%) during the third month in the
organisms in ulcers before and after honey dressing. No ulcer presence of healthy granulation tissue as the size of the ulcer
was completely sterile either at the initial assessment or at the was not expected to heal spontaneously. Another case (3.35%)
end of the study. was grafted, upon the patient request, during the second
Staphylococcus aureus was isolated in 12 patients at the month.
initial assessment (40% of the cases).
At the end of the study, 28 ulcers (93.3%) were colonized by
Staphylococcus epidermidis, while 2 ulcers only (6.7%) were 6. Discussion
colonized by Pseudomonas aeruginosa.
Table 8 shows the overall outcome of honey dressing. There Results proved that honey was an easy-to-use debriding agent.
was significant number of wound completely closed (13 Honey impregnated gauze had rapidly cleaned the wounds

Table 5 – The overall outcome of honey dressing.


Result of dressing 1 month 2 months 3 months Total P-value

N % N % N % N %

Wound closure 4 13.3 4 13.3 5 16.7 13 43.3 0.0089*


Partial healing 0 0 0 0 13 43.3 13 43.3
Amputation 2 6.7 0 0 0 0 2 6.7
Graft 0 0 1 3.35 1 3.35 2 6.7

Mean duration of healing 2.3 weeks


SD 0.94

*
Highly statistical significant at the 0.01 level.
280 diabetes research and clinical practice 89 (2010) 276–281

Table 8 – The overall outcome of honey dressing.


Result of dressing 1 month 2 months 3 months Total P-value

N % N % N % N %

Wound closure 4 13.3 4 13.3 5 16.7 13 43.3 0.0089*


Partial healing 0 0 0 0 13 43.3 13 43.3
Amputation 2 6.7 0 0 0 0 2 6.7
Graft 0 0 1 3.35 1 3.35 2 6.7

Mean duration of healing 2.3 weeks


SD 0.94

*
Highly statistical significant at the 0.01 level.

from debris without the need for enzymatic, chemical or laser therapy [26]). The positive psychological factor as well as
massive mechanical debridement. Wounds were fully deb- cultural and social beliefs explains the variation of clinical
rided as early as the tenth day in 8 patients. By the third week, effectiveness of honey mentioned by Molan [9].
all wounds were grossly debrided. In addition, honey The omnipresence and low price of honey are two
impregnated gauze was easy to prepare (even by the patients important advantages. This was evident in direct cost savings
or their relatives) and to apply. It peeled off easily without pain when compared with conventional and modern dressings;
or damage to the newly forming granulation tissue. Further- 3 kg of honey (enough for 3 months of dressing) was as
more, it was perfect in filling cavities and sinuses within the expensive as 1 l of Povidone Iodine used only for wound
deep diabetic foot wounds. cleansing for less than 1 month. The other important level of
This study revealed rapid diminution of the inflammatory cost reduction was in the rapid healing rates and simplicity of
signs (e.g. edema, hotness and redness) within 10 days in all the technique (dressing was done by patient relatives and at
patients. This was partially due to its anti-edema effect [15] home with no need to go to clinics or import a health
and partially to its antimicrobial effect. In our study, most of professional). More cost saving was through cessation of
the wounds became sterile by the end of the first month of antibiotics use after 1 week in all cases as well as reduction of
honey application. These results were found by Lusby et al. hospitalization period. Further saving of cost was in the
[17] who found that honey was effective against twelve of the reduction of debridement sessions, particularly under general
most common thirteen organisms causing wound infection. anesthesia, skin grafts and amputations.
Furthermore, Maeda et al. found that honey was effective This study demonstrated that honey dressing had no major
against MRSA (methicillin-resistant Staphylococcus aureus) [12]. effect on ulcer with exposed bone. Both amputated cases were
Although P. aeruginosa was still present in 6.7% of wounds, it classified 3-d. The signs of inflammation continued to increase
did not cause any clinical inflammatory manifestations. This and osteomyelitis ultimately developed. Similarly, when there
finding was explained by Lerrer et al. [18] through abrogating was severe vascular insufficiency, honey had no effect.
microbial (particularly P. aeruginosa) adhesion to host cells, Nevertheless, this type of wound showed excellent response
prior to infection establishment. It therefore prevented their to honey dressing after revascularization operation. Although
activity in the wound even when heavily contaminated. there was a good response, bad control of blood glucose level,
No hospital acquired infection was detected in all our series. poor compliance and bad psychological condition markedly
This might be referred to the viscosity of honey, which provided affected the efficiency of honey dressing.
a protective barrier thus preventing cross-infection [9].
All these factors, in addition to the stimulating effect of
honey on granulation tissue and epithelialization [19], resulted 7. Conclusion and recommendations
in rapid absorption of edema (from the wound and surround-
ing area), diminution of discharge, deodorization of the wound Honey is ideal as dressing in cases of diabetic foot wounds
as early as the end of the first week. This rapid dramatic particularly in the developing countries. It is an environmen-
response might explain the perfect patient compliance tally based cost and clinically effective dressing. More
throughout the whole period of the study; proven clinically importantly, it is very safe as it did not result in any
through the absence of dropouts. complication (local or systemic), or emergence of resistant
The psychological factor is an important aspect in bacterial strains. Nevertheless, it is not effective in cases of
improving and impeding immunity and healing power of severe vascular compromise, exposed bone (without perios-
patients [20–23]. As honey is well known in the Egyptian, as tium) or established osteomyelitis.
well as all oriental cultures, as Holy remedy; rendering it a It is indispensable to correct the general condition of the
perfect environmentally based dressing (in concordance with patient to achieve optimum results. Furthermore, patient
patients’ cultural and religious beliefs) that enhanced healing. beliefs and culture should be bared in mind when prescribing
Therefore, the duration of healing in this study was signifi- treatment modalities.
cantly low (mean of 2.3  0.94 weeks) when compared with We recommend a comparative study for comparing the
other modalities (17.7 weeks with conventional dressings [24], results of believers and non-believers of honey as dressing in
15  7 with hyperbaric oxygen [25] and 6–8 weeks with low cases of diabetic foot wound infection.
diabetes research and clinical practice 89 (2010) 276–281 281

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