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The Efficacy and Safety of Natural Honey on the Healing of Foot Ulcers: A
Case Series

Article · April 2015


Source: PubMed

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CASE SERIES

The Efficacy and Safety of Natural


Honey on the Healing of Foot Ulcers:
A Case Series

TE
Hashim Mohamed, MD1; Mansour Abu Salma, RN2; Badriya
Al lenjawi, PhD3; Seham Abdi, RN2; Zaghloul Gouda, RN2;

A
Nour Barakat, MD1; Hisham Elmahdi, MD3; Sisy Abraham,
RN2; Abdul Hakeem Hamza, MD2; Dhyiaa Al Khozaei,
MD2; Shawqia Al Majid, MD2; Hanaa Al Majid, MD2; Johina

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Abdini, MD2; Maryam Al Jaber, MD2; Fareeda Al Masseh, MD2;
Amal Abdulla Al Ali, MD1

Wounds 2015;27(4):103-114

From the 1Weill Cornell Medical


College, Al Rayyan, Qatar; 2Primary
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Abstract: This clinical observation investigated the efficacy, cost-effec-
tiveness, and acceptability of natural honey on the healing of a variety
of chronic foot ulcers at the primary care level. Materials and Meth-
ods. A total of 12 patients with foot ulcers utilizing natural honey as
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Health Care Corporation, Doha, an effective alternative to more expensive, advanced wound products
Qatar; 3Hamad Medical Corporation, were followed. Cases were referred to Umgwailinah Primary Health
Doha, Qatar Care Center, Doha, Qatar from different health centers and from Ha-
D

mad General Hospital, Doha, Qatar. There were also self-referred cases.
Address correspondence to: After rinsing the site with normal saline, natural honey was applied
Hashim Mohamed, MD and the wound was covered by glycerin-impregnated gauze (Adaptic
fmcc2000@gmail.com Non-Adhering Dressing, Systagenix, San Antonio, TX) to prevent the
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absorption of honey into the cotton gauze and away from the wound
site. Patients were followed on a daily basis for an average of 4 weeks.
Disclosure: The authors disclose Results. All ulcers healed with no contractures or scars with a mean
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no financial or other conflicts of healing time of 3 weeks. There was a 75% reduction in the dressing
interest. budget of the health center and a high level of satisfaction among both
health professionals and patients. Patients’ pain levels were reduced
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significantly after using natural honey, as evidenced by the use of the


Visual Analog Scale. Conclusion. The use of natural honey in the man-
agement of chronic foot ulcers proved to be efficacious, cost-effective,
and acceptable by both clinicians and patients.
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Key words: natural honey, efficacy, safety, foot ulcers


D

N
atural honey dressings have been used to treat wounds through-
out the ages.1 This case series describes the use of natural honey
in patients with a variety of chronic foot ulcers. A wound assess-
ment was carried out daily and used to decide upon the continuation of
treatment with natural honey. Numerous preparations of honey have been
Vol. 27, No. 4 April 2015 103
Mohamed et al

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A B C

A
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D
PL E

Figure 1. (A-E) Case 1. Diabetic neuropathic ulcer with 3 weeks time to healing.
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D

A B C
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Figure 2. (A-C) Case 2. Varicose ulcer with 6 weeks time to healing.

previously studied and categorized according to the for stimulating tissue regeneration, debriding necrotic
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floral origin. And while leptospermum honeys are the tissues, reducing edema, and promoting rapid wound
most widely studied,2 a local regional honey was used healing.6,7 Furthermore, natural honey leads to sup-
to treat the patients in this case series. Natural honey pression of inflammation, minimization of scarring, and
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is a viscous, supersaturated sugar solution derived from stimulation of angiogenesis.6 The acidic pH of honey
nectar gathered and modified by the honeybee.3 It has (3.2 to 4.2) inhibits growth of most pathogenic bac-
high osmolarity and acidity, flavonoids,4 beeswax, hy- teria within wounds,8 and increases production of hy-
drogen peroxide, and inhibin. Natural honey has been drogen peroxide from the enzyme glucose oxidase at
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shown to possess antibacterial potency well in excess 1:1000 concentration. This is less than the convention-
of that needed to stop the growth of clinically impor- al rinse solutions but just enough to inhibit bacterial
tant organisms such as methicillin-resistant Staphylo- growth without compromising the new granulation tis-
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coccus aureus and vancomycin-resistant Eschericia sue.9 Natural honey also provides bacteria with glucose
coli.5 and fructose as an alternative to the amino acids from
dead cells and serum, thereby deodorizing infected
Natural Honey in Wound Care wounds.10 Compounds such as ammonia, amines, and
Mechanism of effectiveness. Due to its therapeu- sulphur, which are the cause of malodor in wounds, are
tic characteristics, natural honey has been used in replaced by lactic acids.11,12 According to histological
wound care as a topical treatment for infected wounds studies,13-15 natural honey is thought to possess anti-
104 WOUNDS® www.woundsresearch.com
Mohamed et al

inflammatory properties. The definitive mechanism external pathogens. Also of note is that it causes mini-
is yet to be identified although preliminary data sug- mal pain during application and removal, and maintains
gests natural honey may activate monocytes within the the wound at optimum temperature and pH.23 Natural
wound.16,17 Additionally, natural honey provides mois- honey has a low adherence to the wound bed upon

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ture to wounds, thereby aiding fibroblast migration and removal thereby preserving the newly forming granula-
epithelialization, reducing scarring and hypertrophy,8 tion tissue. In addition to hampering the development
and working as a physical barrier to external patho- of biofilms,20,21 natural honey has a limited keratinocyte
gens, especially when the wax content in the honey is and fibroblast cytotoxicity compared to conventional
high. Furthermore, honey reduces pain and promotes silver dressings.22 It limits the amount of edema,24 im-

A
granulation tissue formation.11,18 Clinical and labora- proves tissue granulation and epithelialization in the
tory data indicate natural honey is effective against a proliferative phase while decreasing total wound heal-
variety of common pathogens such as Staphylococcus ing time,25 and reduces scarring and contractures in

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aureus, Staphylococcus epidermidis, Psuedomonas patients with burn wounds.26 Natural honey lowers the
aeroginosa, Escherichia coli, Klebsiella pneumoni- alkaline pH of wounds, thereby enhancing healing out-
ae,4 Acinetobacter, Stenotrophomonas,19 methicillin- comes,27,28 and deodorizes infected wounds as the ami-
resistant S. aureus, and vancomycin-resistant E. coli.5 no acids from dead cells and serum that cause malodor,
Natural honey with
high wax content forms a
semisolid medium offer-
ing a better wound contact
thereby preventing the de-
velopment of biofilms20,21
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without compromising the
newly forming fibroblasts.
It should also be noted that
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recent in vitro studies have A B


demonstrated limited cyto-
toxicity to human keratino-
cytes and dermal fibroblasts
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when compared to conven-


tional silver dressing.22
Evidence for natural
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honey. Natural honey has


been assessed in many labo-
ratory and clinical studies C D
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and demonstrated an effec- Figure 3. (A-D) Case 3. Diabetic neuropathic ulcer with 8 weeks time to healing.
tive bacterial barrier against
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A B C

Figure 4. (A-C) Case 4. Diabetic neuropathic ulcer with 4 weeks time to healing.

Vol. 27, No. 4 April 2015 105


Mohamed et al

Table 1. Patient and wound characteristics.


Patient Age Wound etiology and Smoking status Wound measurement Previous treatment
number comorbidities at presentation
(L x W x D, cm)

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1 45 Spontaneous, diabetes, Nonsmoker 3.0 x 3.0 x 0.7 Cadexomer iodine paste
hypertension

2 70 Spontaneous, chronic Smoker 3.0 x 2.0 x 0.2 Povidone iodine


venous insufficiency

A
3 55 Trauma, diabetes Smoker 2.5 x 2.0 x 0.5 Hyrogel and nonadherent

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peripheral vascular silver dressing (Nu Gel
disease, hypertension Hydrogel and Silvercel
Non-Adherent Dressing,
Systagenix, Gatwick, UK)
4 65 Spontaneous, coronary Smoker 3.0 x 2.5 x 0.3 Hyrogel and nonadherent

5 70
artery disease,
hypertension, renal
impairment

Traumatic,
diabetes, peripheral
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Nonsmoker 2.5 x 2.5 x 0.3
silver dressing

Silver sulfadiazine
(Flamazine, Smith & Nephew,
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vascular diabetes, St. Petersburg, FL)
hypertension, obesity,
hypercholesterolemia
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6 70 Trauma, diabetes Nonsmoker 4.0 x 1.5 x 1.0 Nonadherent silver dressing


peripheral vascular
disease, hypertension
7 59 Trauma, diabetes, Nonsmoker 3.0 x 1.0 x 0.1 Silver-impregnated dressing
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hypertension (Acticoat Flex 7, Smith &


Nephew, St. Petersburg, FL)
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8 55 Trauma, diabetes Nonsmoker 3.0 x 2.0 x 0.2 Povidone iodine


peripheral vascular
disease, hypertension
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9 47 Thermal burn, contact Nonsmoker 10.0 x 4.0 x 0.1 Dry cotton gauze
dermatitis diabetes,
hypertension
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10 37 Burn, diabetes Nonsmoker 5.0 x 4.0 x 0.2 Dry cotton gauze

11 64 Spontaneous, diabetes, Nonsmoker 1.5 x 1.5 x 1.5 Silver sulfadizine (Allevyn


D

Charcot foot Advanced Foam Wound


Dressing, Smith & Nephew,
St. Petersburg, FL),
nonadherent silver dressing
12 76 Trauma, diabetes Nonsmoker 4.0 x 1.3 x 0.2 Antibacterial spray

*Pain was assessed using the Visual Analogue Scale in which 1 = minimal pain and 10 = maximum pain.

106 WOUNDS® www.woundsresearch.com


Mohamed et al

Duration Glycemic control Infection status Duration Average Pain* before vs


of previous elevated protease of honey epithelialization rate during treatment
wound activity (EPA) treatment

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3 months HbA1C = 7.8% Not infected 3 weeks 1.2 mm per day 1/10 vs 1/10
Suboptimal control

2 months HbA1C = 4% Infected 6 weeks 0.6 mm per day 7/10 vs 1/10


Normal

A
3 months HbA1C = 7.9% Low EPA 8 weeks 0.4 mm per day 1/10 vs 1/10

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Suboptimal control

One month HbA1C = 7.4% Infected 4 weeks 1.1 mm per day 8/10 vs 1/10

2months
Suboptimal control

HbA1C = 7.5%
Suboptimal control
Not infected
PL 3 weeks 1.2 mm per day 1/10 vs 1/10
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D

4 months HbA1C = 7% Low EPA 5 weeks 0.8 mm per day 1/10 vs 1/10
Good control

3 months HbA1C = 6.9% Low EPA 3 weeks 1.1 mm per day 7/10 vs 1/10
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Good control
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2 months HbA1C = 8% Low EPA 2 weeks 1.4 mm per day 2/10 vs 1/10
Suboptimal control
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1 week HbA1C = 8.5% Infected 3 weeks 0.7 mm per day 5/10 vs 1/10
Suboptimal control
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1 week HbA1C = 8% Not infected 1 week 1.9 mm per day 8/10 vs 2/10
Suboptimal control
6 months HbA1C = 8% Not infected 3 weeks 0.55 mm per day 1/10 vs 1/10
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Suboptimal control

1 week HbA1C = 7% Not infected 3 weeks 0.66 mm per day 4/10 vs 1/10
Good control

Vol. 27, No. 4 April 2015 107


Mohamed et al

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A
A B C

Figure 5. (A-C) Case 5. Diabetic neuropathic ulcer with concomitant peripheral artery disease. Time to healing was 3 weeks.

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A B C
Figure 6. (A-C) Case 6. Diabetic neuropathic ulcer with concomitant peripheral artery disease. Time to healing was 5 weeks.
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such as sulphur compounds, ammonia, and amines, the use of natural honey are summarized in Table 1. All
are replaced by lactic acids.29,30 Furthermore, natural patients were treated with topical natural honey pur-
honey debrides slough, stimulates angiogenesis,31-34 chased from the local market. The honey was a homog-
and stimulates immunomodulation by up-regulating tu- enous, thick, white honey mixed with royal jelly and
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mor necrosis factor alpha, interleukin (IL)-1 beta, IL-6, produced by Russian bees (ie, Apis mellifera) native to
and prostaglandin E2 from monocytes.35 Finally, natural the Primorsky Krai region of Russia. Prior to use with
honey is bactericidal and antifungal against approxi- patients, the honey was sent to the microbiology labo-
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mately 70 bacterial strains, both gram-positive and ratory of the Ministry of Health in Qatar. After rigorous
gram-negative, and some yeasts.36,37 testing, it was found to be sterile and free from Clos-
The performance of natural honey was evaluated tridium difficile spores.The wounds were cleaned with
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previously38-40 in a case series that included patients normal saline and surgically debrided using a sharp
with complex comorbid conditions, locally infected scalpel if they had necrotic tissues or callosities until
wounds which failed hospital management including a clean wound bed was achieved (ie, no necrotic tis-
diabetic foot ulcers, postexcisional malignant melano- sue was present). At that point, treatment with natural
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ma ulceration,10 contact dermatitis, burns, and Charcot honey was commenced by applying it directly on the
foot ulceration. There was excellent tolerability, and no wound bed and covering it with a nonadherent dressing
trauma caused to the wound bed. made of knitted cellulose acetate fabric (Adaptic Non-
D

Adhering Dressing, Systagenix, San Antonio, TX) and im-


Materials and Methods pregnated with specially formulated petroleum emul-
Patients. All patients were seen in a primary care sion.When natural honey is applied to the wound bed it
health center (Umgwailinah Primary Health Care Cen- becomes less viscous and is diluted through exudation.
ter, Doha, Qatar) and had been receiving various thera- As a result, wounds were covered with a cotton wool
pies for their chronic and acute wounds. Wound etiolo- bandage and a light crepe bandage to contain the natu-
gies, timelines, and wound products applied prior to ral honey in the wound bed environment. The natural
108 WOUNDS® www.woundsresearch.com
Mohamed et al

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A B C
Figure 7. (A-C) Case 7. Chronic traumatic ulcer with 3 weeks time to healing.

A
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A B
PL C
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Figure 8. (A-C) Case 8. Chronic traumatic ulcer with 2 weeks time to healing.

honey dressing was changed


D

on a daily basis and offload-


ing was provided using a mul-
tilayered incontinence pad
which was applied around
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the periwound area. This op-


tion was chosen since total
contact or removable casts
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are not available at the pri-


mary care level, but only if A B
the patient is admitted to the
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hospital. At each daily review


the wounds were debrided
if necessary and assessed for
signs of infection and pain
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level. No systemic or local an-


tibiotics were administered
except in case 4 which had
D

signs of infection on presen-


tation, and case 9 in which
the patient had sustained a
thermal burn and was started C D
on oral ciprofloxacin to cover
Figure 9. (A-D) Case 9. Contact dermatitis complicated by second degree thermal burn.
for P. aeuroginosa. Time to healing was 3 weeks.
The study consisted of 12
Vol. 27, No. 4 April 2015 109
Mohamed et al

patients with a variety of acute and chronic wounds history, smoking status, clinical history, size of wound,
secondary to type II diabetes, peripheral vascular dis- previous wound products used, duration of wound
ease, chronic venous insufficiency, type I diabetes, and prior to treatment, glycemic control, infection status,
burns, although secondary diagnosis included trau- duration of natural honey application until wound clo-

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ma, contact dermatitis, and Charcot foot. Age, gender, sure, average epithelialization rates calculated from
wound etiology, related comorbidities, pain score, and daily wound dimension measurements, and patients’
wound size are listed in Table 1. Patients were managed reported local pain prior to and during treatment with
according to the etiology of the wound. Treatment in- natural honey. Pain was assessed using the Visual Analog
cluded cleaning with normal saline and sharp debride- Scale (VAS), a unidimensional measure of pain intensity

A
ment of necrotic tissue, application of natural honey which has been widely used in diverse adult popula-
covered by 3 layers of a paraffin-based dressing to pre- tions, including those with chronic painful conditions.
vent absorption of honey onto the secondary cotton The VAS is a continuous scale comprised of a horizon-

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gauze, and offloading. All patients showed complete tal and a vertical line, usually 10 cm in length, anchored
healing with a mean healing time of 3 weeks. by 2 verbal descriptors, one for each extreme. For pain
intensity, the scale is most commonly anchored by “no
Results pain” (score of 1) and “worst imaginable pain” (score
From 2011 to 2014, 12 patients with various chronic of 10).
and acute wounds (Figures 1-12) presented to Umg-
PL Clinically, patients 1, 2, 4, 5, 6, 7, 8, 10, 11, and 12 had
wailinah Primary Health Care Center, Doha, Qatar. They a marked response to the treatment regimen, while pa-
were subsequently managed on an outpatient basis tient 3’s wound failed to respond in such a swift man-
and treated daily with natural honey as previously de- ner, and required about 8 weeks of treatment to achieve
scribed. Table 1 shows ages, wound etiology, clinical complete closure (Table 1). However, it should be
U
noted that patient 3 was a chronic
heavy smoker of 40 cigarettes per
day, with chronic diabetic compli-
D

cations including diabetic retinop-


athy. He also had been living with
hypercholesterolemia and periph-
eral vascular disease. Patient 9 had
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sustained a second degree burn


complicated by cellulitis and the
wound was heavily infected with
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A B a high level of protease activity as


measured by a point of care test
Figure 10. (A-B) Case 10. Second degree thermal burn with 1 week time to healing.
(Woundchek Protease Status test,
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Woundchek Laboratories, North


Yorkshire, UK). The attending
consultant family physician with
a special interest in diabetic foot
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management started the patient


on oral ciprofloxacin, debrided
the wound, took a deep swab, in-
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tensified his insulin regimen, and


ordered a twice-daily dressing
change due to high exudate. These
A B factors produced swift results and
the wound was closed in 3 weeks
Figure 11. (A-B) Case 11. Charcot foot with neuropathic ulcer. Time to healing was
2 weeks. time. Average wound duration pri-
or to the natural honey treatment
110 WOUNDS® www.woundsresearch.com
Mohamed et al

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A B C
Figure12. (A-C) Case 12. Traumatic fish bite with 3 weeks time to healing.

A
for all 12 patients was 120.2 days (range 14-180 days). sided to no activity 2 weeks after beginning treatment

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Average natural honey treatment duration was 23.8 with honey. Patient 4 experienced EPA due to the pres-
days including patients 3 and 9. Average wound epi- ence of osteomyelitis. The EPA dropped 2 weeks post-
thelialization rate was 0.6 mm per day. initiation of systemic ciprofloxacin at presentation and
When comparing local pain symptoms with the nat- then increased again for another week due to the pres-
ural honey treatment regimen compared to previously ence of osteomyelitis as evidenced by a positive probe-
used wound products, 6 patients (patients 2, 4, 5, 6, 7,
and 11) had no local pain symptoms on the VAS before
or during the natural honey treatment, since they had
diabetic peripheral neuropathy and were unable to feel
pain, and patient 11 had Charcot foot. Patient 2 was ex-
PL to-bone test. Clinicians seeing patients in a similar set-
ting (ie, a specialized diabetic foot unit with a high
prevalence of osteomyelitis in the patient population)
can confidently diagnose diabetic foot osteomyelitis
when either the probe-to-bone test or a plain x-ray, or
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periencing a high level of pain measured as a 7 on the especially both, are positive.44 However, after proper
VAS. That score fell to 2 after 1 week of treatment with antibacterial coverage coupled with a natural honey
honey, and to 1 after 6 weeks of treatment with honey. dressing, the EPA became minimal at week 3. Similarly,
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Similarly, patient 4 presented with high intensity pain patient 7 had an elevated EPA, the wound was malodor-
and a score of 8 on the VAS, which dropped to 3 after 1 ous, and necrotic tissue was present in the wound bed.
week of treatment with honey, and to 1 after 2 weeks Amoxicillin clavulanate coupled with natural honey
of treatment with honey. Patient 9 had a VAS score of dressing resulted in the EPA to be brought to a mini-
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5 on presentation which dropped to 1 after 2 weeks mum on week 2. Patient 9, who had a second degree
of treatment with honey. Finally, patient 12 presented burn complicated by cellulitis, had high EPA activity
with a VAS score of 8 and dropped to 2 after 1 week and was prescribed oral ciprofloxacin to cover for P.
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of treatment with natural honey. This finding is quite aeuroginosa; this regimen resulted in the reduction of
encouraging as the pain in wounds results from the the EPA activity to a minimum amount 2 weeks later.
nerve endings being sensitized by prostaglandins pro-
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duced in the process of inflammation, as well from the Discussion


pressure on tissues resulting from edema. Due to its This case series raised many points of interest with
high sugar content, honey also prevents pain during regard to the use of natural honey in wound manage-
dressing changes as it keeps the wound surface moist ment. It was interesting to note there was no report
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by mobilizing the edema from the surrounding tissues. of adverse effects with the use of honey from either
Wound infection status was assessed using a point patients or health professionals. Even stinging sensa-
of care protease status test since, although chronic tion, which had been reported elsewhere27,38 among
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wounds with elevated protease activity (EPA) have a patients with arterial insufficiency, was not reported
90% probability of not healing without appropriate in- in the authors’ patients with peripheral artery disease.
tervention, and 28% of nonhealing wounds have EPA,3 This could be due to the varying pH of different types
there are no visual cues to detect EPA.41-43 Patients 1, 5, of honey, coexistent peripheral neuropathy, and differ-
and 12 had no elevated EPA throughout their treatment ent composition and floral source of the honey used.
regimen while patients 2, 3, 6, 8, and 11 had minimal There are many reports of honey deodorizing mal-
EPA prior to treatment with natural honey which sub- odorous wounds, especially among chronic diabetic
Vol. 27, No. 4 April 2015 111
Mohamed et al

wounds.10,38,45 Health professionals and patients were References


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