1. Scar Quality and Physiologic Barrier Function
Restoration After Moist and Moist-Exposed Dressings
of Partial-Thickness Wounds
BISHARA S. ATIYEH, MD, FACS,n
KUSAI A. EL-MUSA, MD,n
AND RUWAYDA DHAM, PHDw
n
Division of Plastic and Reconstructive Surgery, American University of Beirut Medical Center, Beirut, Lebanon, and
w
Drug Research Center, Dubai, United Arab of Emirates
BACKGROUND. There is growing evidence of improved healing
of full- and partial-thickness cutaneous wounds in wet and
moist environments. Retention of biologic fluids over the
wound prevents desiccation of denuded dermis or deeper
tissues and allows faster and unimpeded migration of kerati-
nocytes over the wound surface. It allows also the naturally
occurring cytokines and growth factors to exert their beneficial
effect on wound contracture and re-epithelialization. Despite all
of these documented benefits, applying the moist healing
principles to large surface areas, in particular to large burns,
is hindered by the major technical handicap of creating and
maintaining a sealed moist environment over these areas.
METHODS. From January to September 2001, healing of
partial-thickness skin graft donor sites was studied in a
prospective comparative study of two types of moist dressings,
Tegaderm (3M Health Care, St. Paul, MN), a semipermeable
membrane occlusive dressing, and moist exposed burn ointment
(MEBO) (Julphar; Gulf Pharmaceutical Industries, United Arab
of Emirates), an ointment that can provide a moist environment
without the need of an overlying occlusive dressing. Healing
was assessed both clinically and with serial measurements of
transepidermal water loss (TEWL) and moisture. Following
healing, scar quality was evaluated by two members of the team
separately using a visual analog scale. Results were statistically
analyzed.
RESULTS. Faster healing was observed clinically with MEBO
application. Physiologic healing as determined by TEWL
measurements occurred at an extremely significant earlier stage
for MEBO, and this was associated with better scar quality,
demonstrating a positive relationship between function and
cosmetic appearance. Moreover, the ointment is definitely easier
to apply than the occlusive self-adhesive membrane, which
requires some degree of dexterity and expertise.
CONCLUSION. MEBO application is an effective and valid
alternative to conventional occlusive dressings. Moreover, the
observed improved anatomic and physiologic healing indicates
that MEBO may have a positive effect on healing more that the
mere fact of passive moisture retention.
B.S. ATIYEH, MD, FACS, K.A. EL-MUSA, AND R. DHAM, PhD HAVE INDICATED NO SIGNIFICANT INTEREST WITH
COMMERCIAL SUPPORTERS.
A WOUND is a tissue disruption of normal anatomic
structure and function. Wound healing, on the other
hand, does not culminate in tissue regeneration but
rather in tissue restoration.1
Healing of open cuta-
neous wounds involves three processes: epithelializa-
tion, connective tissue deposition, and contraction.
The contribution of each process varies according to
the type of wound.2
Epithelialization is the main
healing mechanism of partial-thickness wounds, re-
sulting in restoration of the stratified squamous
epithelium that protects the body from fluid loss,
bacterial invasion, electromagnetic radiation, and
general trauma.3
Ever since Winter4–6
proposed his
classic hypothesis that the optimum environment for
epithelialization is a moist environment, there is more
recent evidence in the literature that good hydration is
the single most important external factor responsible
for optimal wound healing.7–14
Possible mechanisms
explaining the observed improved healing include
easier migration of epidermal cells over the moist
wound surface instead of under a dry scab, increased
partial pressure of oxygen, and the preservation of
growth factors and proteinases present in fluid
exudates that are hence allowed to exert their
potentiating effect on wound healing.8
The clot-
inducing environment caused by increased precipita-
tion of fibrinogen and fibronectin observed under
moist conditions helps also in promoting re-epithelia-
lization.
Moist wound healing is one of the most frequently
used but least understood terms in wound care
nowadays. Although no reliable operational defini-
tions exist of too little or too much wound surface
r 2003 by the American Society for Dermatologic Surgery, Inc. Published by Blackwell Publishing, Inc.
ISSN: 1076-0512/02/$15.00/0 Dermatol Surg 2003;29:14–20
Address correspondence and reprint requests to: Kusai A. El-Musa,
MD, Division of Plastic and Reconstructive Surgery, American
University of Beirut, 18th Floor, 850 3rd Avenue, New York, NY
10022, or e-mail: elmusakusai@hotmail.com.

2. moisture, it is clear that dressings with controlled
permeability provide a protective barrier, prevent
eschar formation, reduce the dermal necrosis seen in
wounds that have been allowed to dry, and signifi-
cantly accelerate wound re-epithelialization.15
Healing
under both wet and moist environments is significantly
faster than under dry conditions. Speed of healing,
however, in moist or wet wounds may not be
significantly different,16
although in an experimental
study, full-thickness wounds of pigs contracted more
and healed faster in wet rather than moist or dry
environments.8
Some have proposed that the optimum
environment would be an intermediate gelatinous
environment between moist and dry such as seen
under highly vapor-permeable dressings,16,17
and even
others have demonstrated accelerated healing of full-
thickness skin wounds in a wet environment in
contradistinction to a moist environment.8
Irrespective
of this apparent controversy, allowing traumatized or
ischemic tissues to dehydrate produces further tissue
loss by transforming the ‘‘zone of stasis’’ adjacent to
the zone of injury into a ‘‘zone of necrosis.’’8,18
Clinical healing of similar wounds during similar time
frames follows patterns predicted by dressing moisture
retention. This observation suggests that when other
variables are held constant, the use of more moisture-
retentive dressings generally achieves environments
supportive of earlier healing outcomes when compared
with less moisture-retentive dressings.15
Enthusiasm
generated by these results has been tempered by
concerns over tissue maceration and infection after
prolonged cutaneous water exposure.5,19
These con-
cerns may not be justified. In fact, prolonged exposure
of skin to physiologic fluids such as amniotic fluid20
or
saline5
does not seem to produce maceration and is not
comparable to the conditions encountered in World
War I associated with trench foot.5
Anyway, macera-
tion may well be an unwelcomed occurrence with
moisture-retentive dressing use on highly exuding
wounds; however, it is not consistently associated with
increased adverse events. Evidence further suggests
that greater dressing moisture retention is associated
with fewer clinical infections, greater patient comfort,
and reduced scarring.15
Although re-epithelialization of partial thickness
wounds constitutes anatomic healing and restoration
of skin integrity, it does not, however, necessarily mean
physiologic healing and recovery of the cutaneous
barrier function. It remains to be determined whether
earlier physiologic healing affects the final outcome of
anatomic healing and scar quality. This question
remains unresolved. It has been though well estab-
lished that altered cutaneous barrier provides access to
infectious organisms and toxins and increases basal
metabolic rate and oxygen demand. Moreover, the
resultant high water loss leads to poor temperature
control and difficulty in fluid balance.21
In a prospective clinical study performed between
January and September 2001, healing of partial-
thickness skin graft donor sites was evaluated under
two different types of moist dressings: Tegaderm (3M
Health Care, St. Paul, MN), a semipermeable mem-
brane conventional moisture retentive dressing, and
moist exposed burn ointment (MEBO; Julphar; Gulf
Pharmaceutical industries), a recently described burn
ointment providing moist environment for optimal
healing without the need of secondary dressing
application. Anatomical healing was assessed clini-
cally, whereas barrier function recovery was mon-
itored by transepidermal water loss (TEWL)
measurements by Dermalab 900 (Denmark). Scar
quality was evaluated by the visual analog scale for
scar assessment described by Beausang et al.22
The
purpose of this study was to determine whether the
two types of moisture retentive dressings produced
comparable anatomic and physiologic healing with
good quality scars as speculated and whether MEBO
could be a valid alternative in the management of large
partial-thickness wounds such as second-degree burns
for which the application of currently available
occlusive moist dressings is not practical or even
associated with a high complication rate.
MEBO is a Chinese burn ointment with a U.S.
patented formulation since 1995. The active compo-
nent of the ointment is -sitosterol in a base of beeswax,
sesame oil, and other components. Clinical and
experimental studies reported in the Chinese literature
have demonstrated that MEBO reduces markedly
evaporation from the wound surface.23
It has an
inhibitory effect on smooth muscle cells that is dose
related24
and has no evident effect on the humoral and
cellular immune defense mechanisms.25
Although
MEBO does not have any demonstrable in vitro
bacteriostatic and bactericidal activity probably be-
cause of its oily composition that does not allow
proper diffusion in a watery culture medium,26,27
it
has been shown that in vivo, it had similar action to
1% silver sulfadiazine in controlling burn wound
sepsis and systemic infection with Pseudomonas
aeroginosa.28
It has also been demonstrated experi-
mentally that MEBO exhibited a statistically signifi-
cant wound healing potential on rabbit corneal
epithelium as compared with saline, homologous
serum, vitamin A, and dexamethasone.29
Moreover,
rabbit skin burns healed at a much faster rate with
better quality scars when treated with MEBO than
similar burns treated with vaseline with demonstrable
histologic differences on repeated serial biopsies.30
The
ointment produces good analgesia and has a good
debriding effect; moreover, it drastically reduces water
Dermatol Surg 29:1:January 2003 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS 15

3. loss and exudation from the open wound surface. The
required frequent application of the ointment is easy
and can be performed by the patient or a member of
his or her family. The most remarkable practical
advantage of MEBO over other types of dressings is
that it provides an effective wet environment favorable
for optimal wound healing without the need of any
covering or occlusive dressing. In some cases, however,
particularly when the patient is not confined in bed or
at home, a simple covering dressing may be more
convenient. In a recent experimental study on pigs31
and another clinical study about the healing of skin
graft donor sites,32,33
MEBO has been shown to
produce fast re-epithelialization and healing with
excellent quality scars. In a recent report, MEBO has
been found to be a useful alternative for the treatment
of partial-thickness facial burns because of its con-
venient method of application that allows easier
assessment of healing progression.34
Methods
Thirteen adult patients with no underlying medical
conditions requiring split-thickness skin grafts to cover
open defects accepted to participate in the study;
0.012-in thick skin grafts were harvested uniformly in
all patients by the same investigator using the Padget
electric dermatome. A total of 20 donor site study
fields were available. They were assigned randomly for
MEBO (10 fields) or Tegaderm (10 fields) application.
In 5 patients, MEBO and Tegaderm could be applied
simultaneously on two separate fields, and in one
additional patient, three donor fields were available
for investigation (Figure 1). The ointment was applied
daily in a thick layer after gently removing the
previously applied layer with sterile gauze, and the
site was covered by a simple semiopen dressing. The
Tegaderm layer, on the other hand, was changed
whenever indicated, either when excessive fluid has
accumulated or fluid leakage has occurred or whenever
the membrane has lost its adherent occlusive property.
Ointment or Tegaderm application was continued
until anatomic healing was observed. Epidemiologic
data regarding age, gender, and skin type were
recorded. Wound healing by surface re-epithelializa-
tion was evaluated qualitatively by clinical assessment
and quantitatively by measuring the wound TEWL as
an indicator of skin barrier function restoration.
Before completion of surface re-epithelialization,
TEWL measurements of the MEBO-treated fields were
made after wiping gently the ointment, while it was
measured over and through the semipermeable mem-
brane or directly on the wound surface whenever the
Tegaderm membrane needed to be changed. The
membrane was not removed intentionally to effect
TEWL measurements in order to avoid any unwar-
ranted injury to the regenerating epithelium. Following
anatomic healing, direct measurement was possible in
all study fields. Three readings were made at each
recording, the average of which was adopted as the
representative measurement. In order to avoid the
wide variation in TEWL caused by ambient tempera-
ture and humidity, the calculated ratio of wound or
subsequent scar TEWL measurement over TEWL of
the adjacent normal skin on any given day was
adopted for statistical analysis. Because of the rela-
tively small number of study fields included in the
study, only nonparametric statistical analysis using the
Mann–Whitney test was possible.
Resultant scar quality was evaluated by two
members of the team separately along a visual analog
scale.40
Scars with total scores of 5 and 6 were
considered to be excellent. Good scars had scores of 7
to 9, fair scars 10 to 14, and poor scars 14 to 18. Total
recorded scores as well as scores of each parameter
(color, contour, distortion, texture, and aspect) were
analyzed independently. Variations over time at 1, 2,
and 6 months within each group were analyzed
statistically using nonparametric repeated-measures
analysis of variance, the Friedman test followed by
Dunn’s multiple comparisons test, which compares
any two particular time points within a particular
Figure 1. Split thickness skin graft (STSG) donor site appearance at
Days 0 (A), 3 (B), and 19 (C).
16 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS Dermatol Surg 29:1:January 2003

4. treatment group. On the other hand, differences
between the two treatment groups at any one
particular time point (months 1, 2, or 6) were analyzed
statistically using nonparametric test, the Mann–
Whitney test, followed by Dunn’s multiple comparison
test.
Results
Because direct biopsy examination is not possible in
this clinical study for obvious reasons, anatomic
healing was determined by clinical observation.
Although definitely not very objective, criteria for
healing included the absence of bleeding or exudating
points and a shiny congruent epithelial covering
sheath. Anatomical healing time for MEBO was
8.972.846 and 13.13472.268 days for Tegaderm.
The observed difference between the two study groups
was significant (P 5 0.0185). It is worth mentioning
that all MEBO-treated areas re-epithelialized unevent-
fully, whereas 3 Tegaderm-covered fields developed
local wound complications. In one case, extensive
granulation tissue developed, necessitating skin graft-
ing. Although initially in the first 3 days TEWL values
in the MEBO-treated group increased sharply from
initial base line values, average TEWL at the time of
anatomic healing was 10.58 and 11.93 times greater
than normal for MEBO and Tegaderm, respectively.
On the other hand, average functional barrier recovery
time was 67.4713.368 days for MEBO and
150746.476 days for Tegaderm (Figure 2). The
difference between the two groups was extremely
significant (P 5 0.0005). Although TEWL measure-
ments through an intact Tegaderm membrane in the
early stages of the study may not give an accurate
reading, this did not have any effect on the validity of
the observed results that were manifested long after
anatomic healing has occurred at a time were both the
ointment and membrane were not in use anymore.
This, however, may have yielded falsely lower TEWL
values, which explains the observed higher TEWL in
the MEBO-treated group as compared with the
Tegaderm group during the first week. Although three
fields in the Tegaderm group developed local wound
complications compared with none in the MEBO
group, the difference in complication rate between the
two groups was not significant (chi-square test and
Fisher’s exact test).
Significantly better scar quality was also observed in
the MEBO group, as evidenced by photographic
documentation and scar assessment scores at 1, 2,
and 6 months (Table 1). Total scores of both treatment
groups are shown in Table 2. Table 3 demonstrates the
significance levels of the observed differences between
the two study groups. The difference at 1 month is
extremely significant (Po0.001). At 2 and 6 months, it
is only significant (Po0.05). On the other hand, a
decrease of total scores over time from month 1 to
month 6 reflecting scar quality improvement was
statistically extremely significant (Po0.001) for
MEBO and very significant (Po0.01) for Tegaderm
(Table 4). Separate score analysis of the various
parameters investigated indicates that contour, texture,
and aspect of the MEBO group did not change
significantly over time, indicating that for these
Table 1. Classification of Scars According to Scar Assessment Scores as E (Excellent), G (Good), F (Fair), and P (Poor)
MEBO Tegaderm
1 Month 2 Months 3 Months 1 Month 2 Months 3 Months
E 20% 60% 90% 0% 10% 40%
G 80% 40% 10% 10% 30% 40%
F 0% 0% 0% 80% 50% 10%
P 0% 0% 0% 10% 10% 10%
Figure 2. Cutaneous functional barrier restoration with Tegaderm and
MEBO.
Dermatol Surg 29:1:January 2003 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS 17

5. parameters the good results were reached at the first
month in contradistinction to the Tegaderm group. No
significant difference (P40.05) was observed regard-
ing distortion between the two groups, although
distortion scores tended to improve with time.
Changes in color scores with time, on the other hand,
were statistically extremely significant (Po0.001) in
the MEBO group and were very significant (Po 0.01)
in the Tegaderm group. Although both treatment
modalities induced a decrease in color counts over
time, it seems that MEBO acted faster than Tegaderm
as the difference in counts between the two was
initially not significant and grew to be significant from
month 2 onward.
Discussion
Wound healing is a complex process to study,
especially in humans because the endpoint(s) of wound
induction and healing is subjective and therefore
difficult to quantitate.35
In studies comparing the
effects of various topical preparations as well as the
effect of various dressing materials on wound healing,
the rate of healing is often judged by clinical
observation of re-epithelialization alone. Although it
Table 2. Descriptive Statistics of the Two Study Groups
(Mean Score7SD at 1, 2, and 6 Months)
Mean7SD
Month 1 Month 2 Month 6
MEBO (N 5 10) 7.370.949 6.670.843 5.570.707
Tegadermn
(N 5 9) 10.471.014 9.0072.062 6.971.691
One patient was excluded from the statistics because of severe complication
requiring skin grafting.
Table 3. Significance of observed differences between the two groups
MEBO Versus Tegaderm
Month 1 Month 2 Month 6
Total nnn n n
Color NS n n
Contour Not possible to analyze data because SD 5 0
Distortion NS NS Identical
Texture Not possible to analyze data because SD 5 0
Aspect Not possible to analyze data because SD 5 0
NS, P40.05.
n
Significant, Po0.05.
nn
Very significant, Po0.01.
nnn
Extremely significant, Po0.001.
Table 4. Nondescriptive Statistics of the Significance Levels Over Time Within Each Study Group
Dunn’s Multiple Comparison Test
Month 1 Versus Month 2 Month 2 Versus Month 6 Month 1 Versus Month 6 Friedman test
(variations with time)
Total MEBO NS n nnn nnn
Tegaderm NS NS nn nnn
Color MEBO NS n nn nnn
Tegaderm NS NS NS nn
Contour MEBO NS NS NS NS
Tegaderm NS NS n nn
Distortion MEBO NS NS NS NS
Tegaderm NS NS NS NS
Texture MEBO NS NS NS NS
Tegaderm NS NS n n
Aspect MEBO NS NS NS NS
Tegaderm NS NS NS nn
NS, P40.05.
n
Significant, Po0.05.
nn
Very significant, Po0.01.
nnn
Extremely significant, Po0.001.
18 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS Dermatol Surg 29:1:January 2003

6. constitutes restoration of anatomical integrity of the
skin, simple re-epithelialization does not necessarily
mean physiologic healing and recovery of the barrier
function of the skin. Restoration of cutaneous barrier
function unfortunately is a property not routinely
assessed.36
Moreover, various noninvasive investiga-
tions of skin morphology and function that are
standard tools to study the pathophysiology of several
cutaneous disorders37
have not been routinely used in
the study of wound healing.
Biopsies, obviously, constitute a more objective
monitoring method to study wound healing namely
re-epithelialization, angiogenesis, and characteristics
of the epidermal–dermal junction. Their invasive
nature, however, precludes their routine application
to most human studies. Measuring protein perme-
ability across the wound surface can monitor re-
epithelialization objectively and reliably. This, how-
ever, is possible only during fluid-phase wound
treatment with an occlusive chamber.5
Evaporimetry,
on the other hand, has been proposed as an alternative
noninvasive technique to assess healing. Although
TEWL measurements correlate very well with
dynamic function testing of the stratum corneum,
namely sorption–desorption, moisture accumulation
tests,38
and skin capacitance measurements,36
they
may not be valid indicators of re-epitheliali-
zation, as TEWL values remain elevated for several
weeks beyond complete epithelial resurfacing.36
TEWL testing is nevertheless a reliable noninvasive
method to evaluate the functional barrier recovery
of skin after wounding and subsequent re-epitheliali-
zation.38–41
The outermost layer of the skin, the stratum
corneum, is the layer that controls the diffusion
and penetration of substances and drugs into and
through the skin39
and functions as an important
barrier to maintain biological homeostasis.42
Surpris-
ingly, knowledge of the stratum corneum structure
and reaction to the various irritants is still poorly
understood. The epidermal lipids, as evidenced
by experimental delipidization,43,44
represent mo-
rphologically the water permeability barrier. The
multilamellar structures formed by intercellular
lipids present in the stratum corneum as well as the
amount of covalently bound ceramides that are
essential for the formation of lamellar structures play
an important role in the maintenance of the barrier
function.42
In the early 1970s, a major revolution in the
management of wounds began. Simple woven absor-
bents that kept the wound as dry as possible were
superseded by occlusive dressings that provided moist
environment for optimal re-epithelialization and
wound healing.45
Semipermeable adhesive membrane
dressing (Tegaderm) and moist-exposed ointment
(MEBO) have been demonstrated to produce a moist
environment favorable for re-epithelialization of
partial thickness wounds.32,33,46
However, dressings
even in the same product category may be asso-
ciated with significantly different environments for
healing.15
The end point of the healing should not be
anatomical healing but rather physiologic functional
healing and restoration of barrier function. The ability
to modulate epidermal barrier function and integrity
relies largely at present on the topical use of protective
materials and substances such as oil-in-oil ointments
and manipulation of the external environment as
practiced in neonatology.47
As understanding of
epidermal barrier development advances, perhaps
pharmacologic manipulation will become a reality.47
Studies in the rat have shown that epidermal barrier
maturation, both structurally and functionally, can be
accelerated by the use of antenatal steroids.48
It is
suggested by this clinical study that MEBO is pointing
in the direction of improved barrier maturation in
human subjects in addition to improved scar quality.
This warrants further investigation with histologic
study of biopsy specimens.
Based on this study, healing of partial thickness
wounds with the two types of moisture-retentive
dressings under investigation was not comparable.
Functional healing as expressed by TEWL was
significantly much faster for the moist-exposed oint-
ment, suggesting a more rapid epithelial maturation
and stratum corneum formation in the MEBO-treated
areas that cannot be explained only by the mere fact of
moisture preservation. It may be due to yet an
unexplored positive action of the ointment promoting
more rapid maturation of the regenerating keratino-
cytes. In that event, the MEBO would be more an
interactive type of dressing rather than a simple
passive dressing that simply retains moisture. MEBO
treatment resulted also in earlier anatomic healing
with significantly superior cosmetic appearance of the
resultant scars over 6 months of follow-up. The study
demonstrates a positive correlation between improved
scar quality and early physiologic recovery of barrier
function, indicating that better cosmesis and improved
function go hand in hand. It is also safe to say that
MEBO is a valid substitute to semipermeable occlusive
dressings.
Acknowledgment The study was presented at the XVI
Congress of International Society of Aesthetic Plastic Surgery
(May 2002, Istanbul, Turkey), at the European Association of
Plastic Surgeons 13th Annual Meeting (May–June 2002,
Crete, Greece), and at the 11th Quadrennial Congress of Inter-
national Society for Burn Injuries (August 2002, Seattle, WA).
Dermatol Surg 29:1:January 2003 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS 19

7. We acknowledge the contribution of Maha Al-Farhan, MPhil,
MBA, in tabulating the data and performing the statistical
analysis.
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20 ATIYEH ET AL.: MOIST AND MOIST-EXPOSED DRESSINGS Dermatol Surg 29:1:January 2003