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Nanomed. J., 3(1): 57-64, Winter 2016
57
The combined effects of Aloe vera gel and silver nanoparticles on wound
healing in rats
1,2,3
Y. Yousefpoor; 1,2*
B. Bolouri; 1
M. Bayati; 3
A. Shakeri; 3
Y. Eskandari Torbaghan
1
Department of Nanotechnology, College of Advanced Sciences and Technology in Medicine, Tehran
University of Medical Sciences, Tehran, Iran
2
Nanomedine Group, College of Applied Advanced Technology in Medicine, Iran University of Medical
Sciences, Tehran, Iran
3
Khalilabad Health Center, Mashhad University of Medical Sciences, Mashhad, Iran
ABSTRACT
Objective(s): This study was aimed at investigating the synergy effects of Aloe vera gel and silver nanoparticles on the
healing rate of the cutting wounds.
Materials and Methods: In order to determine the concentration of silver nanoparticles in Aloe vera gel, the MBC
methods were applied on the most common bacteria infecting wounds, Staphylococcus aureus, Escherichia coli,
Pseudomonas aeruginosa. The cutting wounds with Full-thickness skin were dorsally created on rats; then the rats
were divided into 4 groups. The treatments groups included: mixture ofAloe vera gel and silver nanoparticles, Aloe vera
gel alone and silver nanoparticles alone in addition to control groups. The treatment was carried out for 2 weeks and the
size of the wound closures were measured by an image software analysis.
Results:There was no significant difference (p<0.05) in healing rate between the control and mixture group. However,
there were significant differences between the silver nanoparticles and Aloe vera groups using Tukey’s analysis on the
6th
, 8th
and 10th
days.
Conclusion:The Aloe vera gel increased the rate of wound healing whereas the silver nanoparticles had a delay effect;
and when they were mixed, it was similar to the average effect of both Aloe vera gel and silver nanoparticles.
Keywords: Aloe vera gel, Silver nanoparticle, Wound healing
Nanomed. J., 3(1): 57-64, Winter 2016
DOI: 10.7508/nmj.2016.01.007
*Corresponding Author Email: bolouri.b@iums.ac.ir
Tel: (+98) 915-3336732
Note. This manuscript was submitted on July 19, 2015;
approved on September 25, 2015
Received; 19 July 2015 Accepted; 25 September 2015
INTRODUCTION
Increasing the rate of wound healing in burns and
skin injuries has always been of great interest to medical
professions. Wound healing is a complex process by
which shearing wounds and burn wounds all heal
through the same process [1]. Shear-type wounds, has
little effect on the skin and may lead to epithelial and
connective tissue cells with less interference to the
integrity of the epithelial basement membrane. This is
called a granulation in order to improve the original or
primary. Several factors are causing delays in wound
healing. Insufficient nutritional resources available to
the skin cells, dysfunctional immune system and
presence of an infection which may be the normal flora
or other opportunistic microbes that are in the
environment. The most common infections in the
wounds are caused by Staphylococcus aureus,
Pseudomonas aeruginosa, Enterococcus species and
Escherichia coli [2]. Different course of antibiotic
resistance, especially in methicillin resistant
Staphylococcus aureus (MRSA), methicillin resistance
Staphylococcus epidermidis (MRSE) and vancomycin
resistant demand a new approach to management of
innovative treatments[3].
Aloe vera leaves contain two products. One is the gel,
in the inner side of the leaf and the other is the bitter
yellow juice on the outside of inner layer before the
external covering. Aloe vera gel is composed of 98.5
percent water and it‘s viscous (gel form) due to the
sugar of glucomannan. This gel has about 200 active
ingredients including minerals, vitamins, proteins,
lipids, amino acids and polysaccharides [4]. These
compounds can be noted like acemannan which
ORIGINAL RESEARCH PAPER
Nanomed. J., 3(1): 57-64, Winter 2016
58
Y. Yousefpoor et al.
strengthens the immune system and brady kinase that
has anti-inflammatory properties and magnesium
lactate that reduce itching and the other soothing
and anti-inflammatory such as sialic acid and
antiprostaglandins [5]. The yellow juice contains
anthraquinone glycosides like Aloin, Aloe-emodin,
Barbaloin which are potentially laxative. Effect ofAloe
vera gel for wound healing is to modulate and optimize
the immune system to accelerate wound healing process
[6]. Aloe vera shows a beneficial effect by reducing
the inflammation significantly and providing a more
mature granulation tissue which could accelerate
healing and might produce a sound well-remodeled scar
[7]. It increases the activity of macrophages and
monocytes and stimulation of killer T lymphocytes
which is done through releasing the interleukin 1 and
6, and TNF-α, INF-β, Aloe Vera gel can also block the
production of prostaglandin and thromboxane from
arachidonic acid to reduces inflammation in the wound
[8]. It can also have inhibitory effect against pathogenic
bacteria, causing food poisoning or different diseases
in humans [9]. There are about 200 species of Aloe
vera in the world. Among all, Aloe vera Barbadensis
Miller is the best-known because of being the richest
in useful materials for healing [10]. Nowadays, because
of its antimicrobial activity, the use of silver
nanoparticles (SNPs) has become very widespread[11].
Nano silvers are of various morphologies including
spheres, rods, cubes, triangles, wired and multifaceted
that they all have a size less than 100 nm. Due to their
shape, surface charge, the surface-to-volume
condensation, integrated power and other factors, their
behavior will vary with their surroundings[12]. The
possible mechanism of antimicrobial activity is due to
several effects. SNPs interact with proteins and
enzymes of thiol groups [12], and disrupts processes
such as cell respiration, ion transport across
membranes [13], TheATP production and the ability of
the replication of DNA [14] and block activity of
microorganisms. However, the mechanisms of toxicity
to environment are not very well specified [15]. We
were interested in investigate the effects of Aloe vera
gel and antibacterial properties of SNPs simultaneously
together for wound healing in rats.
MATERIALS AND METHODS
Preparation of Aloe vera gel by filleting technique
Mature leaves of Aloe vera Barbadnsys Miller were
obtained from a greenhouse of medicinal plants
investigation center of jahad university of Kashmar.
Gel of Aloe vera was purified by filleting technique
[16]. After washing and drying the leaves, two cuts
were created parallel to the longitudinal leaf using a
scalpel at the edges of leaves. Cutting the veins in the
transverse direction leads to a combination of bitter
yellow juice withAloe vera gel that is not of our interest.
The leaf epidermis was removed and gel from the leaf
cavities was shaved by a sterile spoon and then
transferred to a sterile blender and was mixed for 5
minutes. By mixing the cells, they rupture and their
content are released.
Then we wait at least for 15 minutes until the foam
reduced and suspended chopped cell pieces
precipitated. Having used a glass funnel and sterile
gauze with holes which can take carcass of the cells,
the gel was filtered into a sterile flask. Then it was
distributed in volumes of 50 ml in sterile plastic
containers with lid and were kept in a freezer (-20 OC
) for
later use.
Determination of concentration of SNPs in Aloe vera
gel
Silver nanoparticles powder was purchased from
Nanostructured & Amorphous Materials (Houston,
TX, USA). These SNPs had 20 nanometers (nm) in size,
-19 millivolts (mv) in zeta potential, 18-22 gr/m2
in
surface area and hydrophilic surfact by Poly vinil
pirolidone 0.3%. A stock concentration (1000 µg/ml)
was made fromthe silver nanoparticles in sterile distilled
water by 10 minutes sonication for next applications.
To determine the minimal bactericidal concentration
(MBC) of SNPs with the least toxicity effects of them,
it was decided to employ the most common bacteria
causing wound infections: Staphylococcus aureus
ATCC 25923, Pseudomonas aeruginosaATCC 27853
and Escherichia coliATCC 25922. Half concentration
McFarland of fresh bacteria in 0.09 % sterile saline
which was equivalent 1.6×108
bacteria per ml was made.
Aloe vera gel with consecutive concentrations of SNPs
in sterile tubes was prepared and 10 microliters of
bacterial suspension equal to 1.6×106
bacteria was
added to 1ml of each sterile tubes, approximately 1.5
million bacteria. The lid tubes were shaken and
incubated at 37°C for 24h. The next day, from each
tube, a small amount of contents was transferred to
blood culture medium [17, 18]. With the addition of 10
µl bacterial suspension to 1ml dilution tubes, 1% error
is caused which is corrected in the dilution. Culture
results in prepared dilutions are shown in Table 1.
Nanomed. J., 3(1): 57-64, Winter 2016
59
Creating wounds and selection of the treatment
groups of rats
This study was conducted on young male Wistar
rats aged 8 to 10 weeks and weighing 250 to 300 g. Rats
were adapted to room conditions after being
transferred, where they were kept in individual cages
for 24 hours. Special conditions of ventilation,
temperature, lighting, humidity, nutrition and safe
drinking water were considered to all the same until
the possible influence of environmental factors in
wound healing between the groups be equal. After a
day, the rats were adapted to the conditions in the
room for a second day, then the rats were anesthetized
for a time of food deprivation and their hairs between
the animal’s shoulders were shaved dorsally on the
surface. An incision with length of 3 centimeters (cm)
and depth of full-thickness on shaved dorsal surface
between the animal’s shoulders was made so that the
incision are not available to the animals. In this kind of
wound both the epidermis and dermis layers were
damaged. Wound areas were nearly 3.7 cm2
on 0th
day.
The animals were randomly divided into 4 groups of 7
rats in each. The control group was (Aor control) treated
with normal saline, the SNPs group was (B or SNPs)
treated with 20 µg/ml of SNPs in sterile distilled water,
The Aloe vera group (C or Alo) treated with Aloe gel
and the mixture group (D or SNPs-Alo) which was
treated with 20 µg/ml of SNPs inAloe vera gel. During
the process of treatment, standard maintenance for rats
was done under the Animal Experiment Regulations.
The dispersion of SNPs in the gel of Aloe vera
After the plastic containers including 50 ml Aloe
vera gel were taken out of the freezer, it was melted and
1 ml SNPs (1000 µg/ml) was added to it and they were
completely mixed. Thus, the concentration of 20 µg/ml
Table 1. The MBC determination of different dilutions of silver NPS
P.aeroginosaE.coliS. aurreusDensity (µg/ml)
---1000
---500
---100
---50
---40
---30
+++20
+++10
+++5
+++1
---Control+ (10000)
+++Control – (0)
SNPs in gel was prepared. To study the dispersion of
the SNPs in Aloe vera gel, Transmission Electron
Microscope images were taken as shown in Fig 1.
Treatment of wound area
The rats were received treatment by seeping the
lotion on the wound twice daily, once 0.5 ml and then 1
ml. Wounds area measurements were done on even
d a y s i n t e r m s o f s q u a r e c e n t i m e t e r ( c m
2
) with using a
high-quality digital camera and Image Analysis
Software(Digimizer.v4.1.1.0).
By a scale ruler four photos were taken from each
wound and was used to measure average. Information
related to reduction of wound area and their
measurements are shown in Table 2. Also Percentage
of Wound Healing (PWH) was calculated which are
shown in Table 3. PWH was calculated by the following
formula.
Percentage of wound healing (PWH) on Χ day = 100 -
Percentage of wound on Χ day
Percentage of wound on Χ day = (Wound area on Χ
day / Wound area on zero day) × 100
When the wound area was reduced to zero (full wound
closure) and full recovery was achieved, randomly 3
samples of each group from the improved wound skin
were biopsied up for histoloegical examination.
Samples were stained by Hematoxylin-Eosin staining,
and they were evaluated in terms of factors Table 4.
Statistical analysis
The calculations were performed using IBM SPSS
Statistics 19 software. To determine differences of
reduction of the wounds area between groups and
assessing their improvement,ANOVAand Tukey’s test
with a significance level of p<0.05 were used with
control and two by two.
Nanomed. J., 3(1): 57-64, Winter 2016
60
The combined effects of Aloe vera gel and silver nanoparticles on wound healing
Fig. 1. TEM images of SNPs present in gel of Aloe vera
Table 2. Reduction of wounds area on different days
Groups n=7
Woundarea
on day 0
Woundarea
on day 2
Woundarea
on day 4
Woundarea
on day 6
Woundarea
on day 8
Woundarea
on day 10
Woundarea
on day 12
Woundarea
on day 14
Control A 3.729±0.36 2.854± 0.29 1.669± 0.24 0.855±0.12 0.478 ± 0.08 0.201 ± 0.1 0.087± 0.07 0.008
SNPs B 3.779 ± 0.1 2.949± 0.19 1.791± 0.33 1.041±0.18 0.628 ± 0.11 0.278± 0.06 0.075 ± 0.4 0.006
Alo C 3.718±0.17 2.583± 0.12 1.473± 0.23 0.608±0.13 0.295 ± 0.13 0.074± 0.03 0.001± .003 0
SNPs-Alo D 3.691±0.29 2.584± 0.31 1.493± 0.26 0.848±0.26 0.366 ± 0.16 0.169± 0.06 0.057± 0.05 0.003
Table 3. Percentage of wound healing (PWH) on different days
Groups n=7
PWH on
day 0
PWH on
day2
PWH on
day4
PWH on
day6
PWH on
day8
PWH on
day10
PWH on
day12
PWH on
day14
Control A 0 22.6 ± 0.29 54.9 ± 0.28 76.9 ± 0.11 87 ± 0.09 94.5 ± 0.1 97.7 ± 0.08 99.9
SNPs B 0 22 ± 0.18 52.7 ± 0.31 72.5 ± 0.16 83.4 ± 0.12 92.7 ± 0.07 97.2 ± 0.5 99.7
Alo C 0 30.5 ± 0.15 60.4 ± 0.21 83.6 ± 0.15 92.1 ± 0.1 98 ± 0.04 100 100
SNPs-Alo D 0 29.7 ± 0.28 59.4 ± 0.27 77 ± 0.24 90.1 ± 0.14 95.4 ± 0.08 98.5 ± 0.06 99.9
Nanomed. J., 3(1): 57-64, Winter 2016
61
Table 4 . Result of histological examination
Groups
Sampels(n=3)
Hemosiderin
Exedateleukocyte
Granulation
Fibrocyte
Epithelialization
Control
A1 Yes No Yes Yes Complete
A2 Yes No Yes Yes Complete
A3 Yes No Yes Yes Complete
SNPs
B1 Yes No Yes Yes No
B2 Yes No Yes Yes No
B3 Yes No Yes Yes No
Alo
C1 Yes No Yes Yes Complete
C2 Yes Yes Yes Yes Complete
C3 Yes No Yes Yes Complete
SNPs -Alo
D1 Yes No Yes Yes No
D2 Yes No Yes Yes Complete
D3 Yes No Yes Yes Defect
RESULTS
When SNPs mix with Aloe vera gel, probably due
to inorganic and organic compounds in gel and changes
in surface charge of them, some of SNPs can stick
together which seen in Fig 1. But antibacterial effects
of SNPs were evaluated on this gel. Therefore, in order
to determine the concentration of SNPs in Aloe vera
gel, MBC method was used which is shown in Table 1.
Thus, the concentrations of 20 μg/ml SNPs in Aloe
vera gel were used to prepare the mixture gel. By this
method, it has been shown that each 1 mlAloe vera gel
containing20 µg SNPs (20 nm)can nearlykill1.5 million
bacteria. This number of bacterial has been selected as
a default from infection. On the other, because of
toxicity in SNPs, high concentrations of SNPs could
not be used. Table 2 shows reduction of wounds area
on even days. Wounds area were nearly 3.7 cm2
on 0th
day. Table 3 shows PWH on even days which they are
0 % on 0th
day. Figs 2 and 3 show the data of Table 2
and 3. All the groups were compared statistically with
the control group and two by two. Aloe group (C) was
treated 2 days earlier than the control group (A) in 12th
days. SNPs-Alo group (D) and control group (A) were
treated at the same time in 14th
days. SNPs group (B)
was treated later than other groups in 15th
days. The
rate of healing between groups were Alo (C) > SNPs-
Alo (D) = Control (A) > SNPs (B). In order to better
compare the curves in Figs 2&3 and verification
accelerate wounds healing between groups, trendlines
were used. There is no a significant difference (p<0.05)
in wound healing between control (A) and SNPs-Alo
(D) groups, but there are significant differences
between SNPs (B) and Aloe (C) groups on days of 6, 8
and 10 as well as between control (A) and Aloe (C)
groups on days 10 and 12. There is also a significant
difference between SNPs (B) and SNPs-Alo (D) groups
on day 8. After full recovery, 3 rats were randomly
selected and samples were taken for histological
testing. Table 4 shows histological hemosiderin
deposition and formation of granulation tissue and
fibroblasts occurred in tissue formation equally in all
groups. But it shows differences between their
epithelialization processes. It was complete inAloe (C)
and control (A) groups and there isn‘t in the SNPs (B)
group and nearly complete or defect in the SNPs-Alo
(D) group. Fig 4 is optical microscopy images of cells
of wounds which stained with Hematoxylin-Eosin.
During treatment and healing of wounds, ulcers
abnormalities were not observed and all rats were
treated in the normal way.
DISCUSSIONS
Fig1 shows the transmission electron microscopy
images of Aloe vera gel containing SNPs indicating
the aggregation of SNPs. This means that Aloe vera
gel has the potential to aggregate SNPs together that
it could be due to changes in surface charge of them.
The charged or non-charged amino acids, organic
acids, mineral elements that had participated in the aloe
gel such as arginine, asparagine, glutamic acid, aspartic
acid, salicilic acid, calcium, iron,zinc, copper and else
[19,20].
Nanomed. J., 3(1): 57-64, Winter 2016
62
Y. Yousefpoor et al.
Fig. 2. Reduction of wounds area from 3.7 cm2
to zero on even days with trendlines
0.000
0.500
1.000
1.500
2.000
2.500
3.000
3.500
4.000
Day0 Day2 Day4 Day6 Day8 Day10 Day12 Day14
Control
SNPs
Alo
SNPs-Alo
Linear (Control)
Linear (SNPs)
Linear (Alo)
Linear (SNPs-Alo)
Fig. 3. Percentage of wound healing (PWH) from 0 to 100% on even days with trendlines
0
20
40
60
80
100
Day0 Day2 Day4 Day6 Day8 Day10 Day12 Day14
Control
SNPs
Alo
SNPs-Alo
Linear (Control)
Linear (SNPs)
Linear (Alo)
Linear (SNPs-Alo)
B2- Hemorrhage A2-Granulation tissue B1- Hemosiderin deposites
A1-Fibrous tissue A2- Epithelialization C1-Complete Epithelialization
C2- Fibrinoleukocytic exudate A1- Epithelialization B1- Granulation tissue
Fig. 4. Optical Microscopy images of cells obtained from wounds and stained with Hematoxylin-Eosin
Nanomed. J., 3(1): 57-64, Winter 2016
63
But it is certain that MBC test is done by the same
mixed gel with connected particles. Result of this
research shows that the Aloe vera gel accelerates
wound healing, as in several studies have been
investigated [21-24]. In several studies, good results
have been taken from the SNPs along with other
materials [7, 25-28]. However, this study shows that
SNPs partly reduce rate of wound healing especially
alone. It can be due to several effects of SNPs that
interact with cells they are recovering. Asha Rani & et
(2008) in a study on the toxicity of SNPs on the genome
of human cells to conclude that SNPs enter to the cell
and the nucleus and binding to the genetic material
and they arrest cell cycle in the G2 phase of mitosis
which can cause damage to cells, So it is possible that
the lack of epithelialization in the SNPs (B) group is
due to this action [29].
This means that toxicity effects of SNPs on the
proliferation of epithelial cells in mitosis lead to the
delayed recovery.According to Table 4, only complete
epithelialization process can be observed in the control
(A) and Aloe (C) groups, it is not formed in the SNPs
(B) group and it was on average defective in the mixed
(D) group. Chen et al [12] in 2008 in a study on the
toxicity of SNPs concluded that SNPs cause a sharp
decrease in mitochondrial activity and lead to cell
malfunction. It has been found that silver ions seems
to perturb mitochondria through interactions with thiol
groups of the mitochondrial inner membrane.As these
effects of silver ions could be completely blocked by
sulfhydryl reagents, (e.g. reduced glutathione (GSH)),
the ûndings clearly suggested that mitochondria were
under oxidative stress when the cells were exposed to
silver ions [12]. In conclusion, a preliminary outcome
of this study could be that SNPs may interact with
proteins and enzymes containing thiol groups such as
glutathione, thioredoxin, SOD and thioredoxin
peroxidase, are key components of the cell’s antioxidant
defense mechanism and are responsible for neutralizing
the oxidative stress of ROS largely generated by
mitochondrial energy metabolism.
SNPs may deplete the antioxidant defense mechanism
which leads to ROS accumulationAccumulation of ROS
could initiate perturbation and destruction of the
mitochondria as shown in Table 4 [12, 30]. According
to the investigated subjects, SNPs do not appear to
increase wound healing as obtained in this study. In
fact, it could be suggested that SNPs have delayed
wound healing process. In the case of epithelialization
defects in group treated with SNPs-Alo mixture, it could
be suggested that the Aloe vera gel increased the rate
of wound healing whereas SNPs decrease it, but the
mixture of SNPs and Aloe gel has produced an effect
which was the sum of each component of the mixture
as shown in Figs 2 and 3. Perhaps the mixed gel had no
effect on recovery, however, it is recommended for
cases such as topical use in wound with severe
infection, in patients with immunodeficiency who have
wound or want to prevent ulcer formation such as
Diabetic Foot, drug resistances and development of
potential anti-bacterial biofilm for various biomedical
and environmental applications against MRSA and
MRSE[26].
CONCLUSION
It could be concluded thatAloe vera gel is effective
in speeding up the wound healing process but when
mixed with SNPs, no significant improvement was
observed in the healing rate.
ACKNOWLEDGEMENTS
We would like to extend our sincere thanks to those
who collaborated including Prof. Ahmadian & Mrs
Shafiizadeh of IBB Research Institute of Tehran
University. Mr Ehsan Ghoddousi of Medicinal Plants
Investigations Center of Jahad University of Kashmar
for providing Aloe vera plant. We also appreciate Mr
Javad Akhtari and Mrs Fatemeh Gheybi at BuAli
Research Institute and Mrs Maasome Mazandarani at
Dr. Shakeri PathobiologyLaboratory. The current study
was derived from an MSc thesis.
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How to cite this article:
Yousefpoor Y, Bolouri B, Bayati M, Shakeri A, Eskandari torbaghan Y. The combined effects of Aloe vera gel and silver nanoparticles on
wound healing in rats. Nanomed. J., 2016; 3(1): 57-64.
DOI:10.7508/nmj.2016.01.007
URL:http://nmj.mums.ac.ir/article_6197_888.html
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[27] Chowdhury S, De M, Guha R, Batabyal S, Samanta I,
Hazra SK, et al. Influence of silver nanoparticles on
postsurgical wound healing following topical application.
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[28] Habiboallah G, Mahdi Z, Majid Z, Nasroallah S, Taghavi
AM, Forouzanfar A, et al. Enhancement of gingival wound
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[29] AshaRani P, Low Kah Mun G, Hande MP, Valiyaveettil
S.Cytotoxicity and genotoxicity of silver nanoparticles
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[30] Singh M, Singh S, Prasad S, Gambhir I. Nanotechnology
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The combined effects of Aloe vera gel and silver nanoparticles on wound healing in rats

  • 1. Nanomed. J., 3(1): 57-64, Winter 2016 57 The combined effects of Aloe vera gel and silver nanoparticles on wound healing in rats 1,2,3 Y. Yousefpoor; 1,2* B. Bolouri; 1 M. Bayati; 3 A. Shakeri; 3 Y. Eskandari Torbaghan 1 Department of Nanotechnology, College of Advanced Sciences and Technology in Medicine, Tehran University of Medical Sciences, Tehran, Iran 2 Nanomedine Group, College of Applied Advanced Technology in Medicine, Iran University of Medical Sciences, Tehran, Iran 3 Khalilabad Health Center, Mashhad University of Medical Sciences, Mashhad, Iran ABSTRACT Objective(s): This study was aimed at investigating the synergy effects of Aloe vera gel and silver nanoparticles on the healing rate of the cutting wounds. Materials and Methods: In order to determine the concentration of silver nanoparticles in Aloe vera gel, the MBC methods were applied on the most common bacteria infecting wounds, Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa. The cutting wounds with Full-thickness skin were dorsally created on rats; then the rats were divided into 4 groups. The treatments groups included: mixture ofAloe vera gel and silver nanoparticles, Aloe vera gel alone and silver nanoparticles alone in addition to control groups. The treatment was carried out for 2 weeks and the size of the wound closures were measured by an image software analysis. Results:There was no significant difference (p<0.05) in healing rate between the control and mixture group. However, there were significant differences between the silver nanoparticles and Aloe vera groups using Tukey’s analysis on the 6th , 8th and 10th days. Conclusion:The Aloe vera gel increased the rate of wound healing whereas the silver nanoparticles had a delay effect; and when they were mixed, it was similar to the average effect of both Aloe vera gel and silver nanoparticles. Keywords: Aloe vera gel, Silver nanoparticle, Wound healing Nanomed. J., 3(1): 57-64, Winter 2016 DOI: 10.7508/nmj.2016.01.007 *Corresponding Author Email: bolouri.b@iums.ac.ir Tel: (+98) 915-3336732 Note. This manuscript was submitted on July 19, 2015; approved on September 25, 2015 Received; 19 July 2015 Accepted; 25 September 2015 INTRODUCTION Increasing the rate of wound healing in burns and skin injuries has always been of great interest to medical professions. Wound healing is a complex process by which shearing wounds and burn wounds all heal through the same process [1]. Shear-type wounds, has little effect on the skin and may lead to epithelial and connective tissue cells with less interference to the integrity of the epithelial basement membrane. This is called a granulation in order to improve the original or primary. Several factors are causing delays in wound healing. Insufficient nutritional resources available to the skin cells, dysfunctional immune system and presence of an infection which may be the normal flora or other opportunistic microbes that are in the environment. The most common infections in the wounds are caused by Staphylococcus aureus, Pseudomonas aeruginosa, Enterococcus species and Escherichia coli [2]. Different course of antibiotic resistance, especially in methicillin resistant Staphylococcus aureus (MRSA), methicillin resistance Staphylococcus epidermidis (MRSE) and vancomycin resistant demand a new approach to management of innovative treatments[3]. Aloe vera leaves contain two products. One is the gel, in the inner side of the leaf and the other is the bitter yellow juice on the outside of inner layer before the external covering. Aloe vera gel is composed of 98.5 percent water and it‘s viscous (gel form) due to the sugar of glucomannan. This gel has about 200 active ingredients including minerals, vitamins, proteins, lipids, amino acids and polysaccharides [4]. These compounds can be noted like acemannan which ORIGINAL RESEARCH PAPER
  • 2. Nanomed. J., 3(1): 57-64, Winter 2016 58 Y. Yousefpoor et al. strengthens the immune system and brady kinase that has anti-inflammatory properties and magnesium lactate that reduce itching and the other soothing and anti-inflammatory such as sialic acid and antiprostaglandins [5]. The yellow juice contains anthraquinone glycosides like Aloin, Aloe-emodin, Barbaloin which are potentially laxative. Effect ofAloe vera gel for wound healing is to modulate and optimize the immune system to accelerate wound healing process [6]. Aloe vera shows a beneficial effect by reducing the inflammation significantly and providing a more mature granulation tissue which could accelerate healing and might produce a sound well-remodeled scar [7]. It increases the activity of macrophages and monocytes and stimulation of killer T lymphocytes which is done through releasing the interleukin 1 and 6, and TNF-α, INF-β, Aloe Vera gel can also block the production of prostaglandin and thromboxane from arachidonic acid to reduces inflammation in the wound [8]. It can also have inhibitory effect against pathogenic bacteria, causing food poisoning or different diseases in humans [9]. There are about 200 species of Aloe vera in the world. Among all, Aloe vera Barbadensis Miller is the best-known because of being the richest in useful materials for healing [10]. Nowadays, because of its antimicrobial activity, the use of silver nanoparticles (SNPs) has become very widespread[11]. Nano silvers are of various morphologies including spheres, rods, cubes, triangles, wired and multifaceted that they all have a size less than 100 nm. Due to their shape, surface charge, the surface-to-volume condensation, integrated power and other factors, their behavior will vary with their surroundings[12]. The possible mechanism of antimicrobial activity is due to several effects. SNPs interact with proteins and enzymes of thiol groups [12], and disrupts processes such as cell respiration, ion transport across membranes [13], TheATP production and the ability of the replication of DNA [14] and block activity of microorganisms. However, the mechanisms of toxicity to environment are not very well specified [15]. We were interested in investigate the effects of Aloe vera gel and antibacterial properties of SNPs simultaneously together for wound healing in rats. MATERIALS AND METHODS Preparation of Aloe vera gel by filleting technique Mature leaves of Aloe vera Barbadnsys Miller were obtained from a greenhouse of medicinal plants investigation center of jahad university of Kashmar. Gel of Aloe vera was purified by filleting technique [16]. After washing and drying the leaves, two cuts were created parallel to the longitudinal leaf using a scalpel at the edges of leaves. Cutting the veins in the transverse direction leads to a combination of bitter yellow juice withAloe vera gel that is not of our interest. The leaf epidermis was removed and gel from the leaf cavities was shaved by a sterile spoon and then transferred to a sterile blender and was mixed for 5 minutes. By mixing the cells, they rupture and their content are released. Then we wait at least for 15 minutes until the foam reduced and suspended chopped cell pieces precipitated. Having used a glass funnel and sterile gauze with holes which can take carcass of the cells, the gel was filtered into a sterile flask. Then it was distributed in volumes of 50 ml in sterile plastic containers with lid and were kept in a freezer (-20 OC ) for later use. Determination of concentration of SNPs in Aloe vera gel Silver nanoparticles powder was purchased from Nanostructured & Amorphous Materials (Houston, TX, USA). These SNPs had 20 nanometers (nm) in size, -19 millivolts (mv) in zeta potential, 18-22 gr/m2 in surface area and hydrophilic surfact by Poly vinil pirolidone 0.3%. A stock concentration (1000 µg/ml) was made fromthe silver nanoparticles in sterile distilled water by 10 minutes sonication for next applications. To determine the minimal bactericidal concentration (MBC) of SNPs with the least toxicity effects of them, it was decided to employ the most common bacteria causing wound infections: Staphylococcus aureus ATCC 25923, Pseudomonas aeruginosaATCC 27853 and Escherichia coliATCC 25922. Half concentration McFarland of fresh bacteria in 0.09 % sterile saline which was equivalent 1.6×108 bacteria per ml was made. Aloe vera gel with consecutive concentrations of SNPs in sterile tubes was prepared and 10 microliters of bacterial suspension equal to 1.6×106 bacteria was added to 1ml of each sterile tubes, approximately 1.5 million bacteria. The lid tubes were shaken and incubated at 37°C for 24h. The next day, from each tube, a small amount of contents was transferred to blood culture medium [17, 18]. With the addition of 10 µl bacterial suspension to 1ml dilution tubes, 1% error is caused which is corrected in the dilution. Culture results in prepared dilutions are shown in Table 1.
  • 3. Nanomed. J., 3(1): 57-64, Winter 2016 59 Creating wounds and selection of the treatment groups of rats This study was conducted on young male Wistar rats aged 8 to 10 weeks and weighing 250 to 300 g. Rats were adapted to room conditions after being transferred, where they were kept in individual cages for 24 hours. Special conditions of ventilation, temperature, lighting, humidity, nutrition and safe drinking water were considered to all the same until the possible influence of environmental factors in wound healing between the groups be equal. After a day, the rats were adapted to the conditions in the room for a second day, then the rats were anesthetized for a time of food deprivation and their hairs between the animal’s shoulders were shaved dorsally on the surface. An incision with length of 3 centimeters (cm) and depth of full-thickness on shaved dorsal surface between the animal’s shoulders was made so that the incision are not available to the animals. In this kind of wound both the epidermis and dermis layers were damaged. Wound areas were nearly 3.7 cm2 on 0th day. The animals were randomly divided into 4 groups of 7 rats in each. The control group was (Aor control) treated with normal saline, the SNPs group was (B or SNPs) treated with 20 µg/ml of SNPs in sterile distilled water, The Aloe vera group (C or Alo) treated with Aloe gel and the mixture group (D or SNPs-Alo) which was treated with 20 µg/ml of SNPs inAloe vera gel. During the process of treatment, standard maintenance for rats was done under the Animal Experiment Regulations. The dispersion of SNPs in the gel of Aloe vera After the plastic containers including 50 ml Aloe vera gel were taken out of the freezer, it was melted and 1 ml SNPs (1000 µg/ml) was added to it and they were completely mixed. Thus, the concentration of 20 µg/ml Table 1. The MBC determination of different dilutions of silver NPS P.aeroginosaE.coliS. aurreusDensity (µg/ml) ---1000 ---500 ---100 ---50 ---40 ---30 +++20 +++10 +++5 +++1 ---Control+ (10000) +++Control – (0) SNPs in gel was prepared. To study the dispersion of the SNPs in Aloe vera gel, Transmission Electron Microscope images were taken as shown in Fig 1. Treatment of wound area The rats were received treatment by seeping the lotion on the wound twice daily, once 0.5 ml and then 1 ml. Wounds area measurements were done on even d a y s i n t e r m s o f s q u a r e c e n t i m e t e r ( c m 2 ) with using a high-quality digital camera and Image Analysis Software(Digimizer.v4.1.1.0). By a scale ruler four photos were taken from each wound and was used to measure average. Information related to reduction of wound area and their measurements are shown in Table 2. Also Percentage of Wound Healing (PWH) was calculated which are shown in Table 3. PWH was calculated by the following formula. Percentage of wound healing (PWH) on Χ day = 100 - Percentage of wound on Χ day Percentage of wound on Χ day = (Wound area on Χ day / Wound area on zero day) × 100 When the wound area was reduced to zero (full wound closure) and full recovery was achieved, randomly 3 samples of each group from the improved wound skin were biopsied up for histoloegical examination. Samples were stained by Hematoxylin-Eosin staining, and they were evaluated in terms of factors Table 4. Statistical analysis The calculations were performed using IBM SPSS Statistics 19 software. To determine differences of reduction of the wounds area between groups and assessing their improvement,ANOVAand Tukey’s test with a significance level of p<0.05 were used with control and two by two.
  • 4. Nanomed. J., 3(1): 57-64, Winter 2016 60 The combined effects of Aloe vera gel and silver nanoparticles on wound healing Fig. 1. TEM images of SNPs present in gel of Aloe vera Table 2. Reduction of wounds area on different days Groups n=7 Woundarea on day 0 Woundarea on day 2 Woundarea on day 4 Woundarea on day 6 Woundarea on day 8 Woundarea on day 10 Woundarea on day 12 Woundarea on day 14 Control A 3.729±0.36 2.854± 0.29 1.669± 0.24 0.855±0.12 0.478 ± 0.08 0.201 ± 0.1 0.087± 0.07 0.008 SNPs B 3.779 ± 0.1 2.949± 0.19 1.791± 0.33 1.041±0.18 0.628 ± 0.11 0.278± 0.06 0.075 ± 0.4 0.006 Alo C 3.718±0.17 2.583± 0.12 1.473± 0.23 0.608±0.13 0.295 ± 0.13 0.074± 0.03 0.001± .003 0 SNPs-Alo D 3.691±0.29 2.584± 0.31 1.493± 0.26 0.848±0.26 0.366 ± 0.16 0.169± 0.06 0.057± 0.05 0.003 Table 3. Percentage of wound healing (PWH) on different days Groups n=7 PWH on day 0 PWH on day2 PWH on day4 PWH on day6 PWH on day8 PWH on day10 PWH on day12 PWH on day14 Control A 0 22.6 ± 0.29 54.9 ± 0.28 76.9 ± 0.11 87 ± 0.09 94.5 ± 0.1 97.7 ± 0.08 99.9 SNPs B 0 22 ± 0.18 52.7 ± 0.31 72.5 ± 0.16 83.4 ± 0.12 92.7 ± 0.07 97.2 ± 0.5 99.7 Alo C 0 30.5 ± 0.15 60.4 ± 0.21 83.6 ± 0.15 92.1 ± 0.1 98 ± 0.04 100 100 SNPs-Alo D 0 29.7 ± 0.28 59.4 ± 0.27 77 ± 0.24 90.1 ± 0.14 95.4 ± 0.08 98.5 ± 0.06 99.9
  • 5. Nanomed. J., 3(1): 57-64, Winter 2016 61 Table 4 . Result of histological examination Groups Sampels(n=3) Hemosiderin Exedateleukocyte Granulation Fibrocyte Epithelialization Control A1 Yes No Yes Yes Complete A2 Yes No Yes Yes Complete A3 Yes No Yes Yes Complete SNPs B1 Yes No Yes Yes No B2 Yes No Yes Yes No B3 Yes No Yes Yes No Alo C1 Yes No Yes Yes Complete C2 Yes Yes Yes Yes Complete C3 Yes No Yes Yes Complete SNPs -Alo D1 Yes No Yes Yes No D2 Yes No Yes Yes Complete D3 Yes No Yes Yes Defect RESULTS When SNPs mix with Aloe vera gel, probably due to inorganic and organic compounds in gel and changes in surface charge of them, some of SNPs can stick together which seen in Fig 1. But antibacterial effects of SNPs were evaluated on this gel. Therefore, in order to determine the concentration of SNPs in Aloe vera gel, MBC method was used which is shown in Table 1. Thus, the concentrations of 20 μg/ml SNPs in Aloe vera gel were used to prepare the mixture gel. By this method, it has been shown that each 1 mlAloe vera gel containing20 µg SNPs (20 nm)can nearlykill1.5 million bacteria. This number of bacterial has been selected as a default from infection. On the other, because of toxicity in SNPs, high concentrations of SNPs could not be used. Table 2 shows reduction of wounds area on even days. Wounds area were nearly 3.7 cm2 on 0th day. Table 3 shows PWH on even days which they are 0 % on 0th day. Figs 2 and 3 show the data of Table 2 and 3. All the groups were compared statistically with the control group and two by two. Aloe group (C) was treated 2 days earlier than the control group (A) in 12th days. SNPs-Alo group (D) and control group (A) were treated at the same time in 14th days. SNPs group (B) was treated later than other groups in 15th days. The rate of healing between groups were Alo (C) > SNPs- Alo (D) = Control (A) > SNPs (B). In order to better compare the curves in Figs 2&3 and verification accelerate wounds healing between groups, trendlines were used. There is no a significant difference (p<0.05) in wound healing between control (A) and SNPs-Alo (D) groups, but there are significant differences between SNPs (B) and Aloe (C) groups on days of 6, 8 and 10 as well as between control (A) and Aloe (C) groups on days 10 and 12. There is also a significant difference between SNPs (B) and SNPs-Alo (D) groups on day 8. After full recovery, 3 rats were randomly selected and samples were taken for histological testing. Table 4 shows histological hemosiderin deposition and formation of granulation tissue and fibroblasts occurred in tissue formation equally in all groups. But it shows differences between their epithelialization processes. It was complete inAloe (C) and control (A) groups and there isn‘t in the SNPs (B) group and nearly complete or defect in the SNPs-Alo (D) group. Fig 4 is optical microscopy images of cells of wounds which stained with Hematoxylin-Eosin. During treatment and healing of wounds, ulcers abnormalities were not observed and all rats were treated in the normal way. DISCUSSIONS Fig1 shows the transmission electron microscopy images of Aloe vera gel containing SNPs indicating the aggregation of SNPs. This means that Aloe vera gel has the potential to aggregate SNPs together that it could be due to changes in surface charge of them. The charged or non-charged amino acids, organic acids, mineral elements that had participated in the aloe gel such as arginine, asparagine, glutamic acid, aspartic acid, salicilic acid, calcium, iron,zinc, copper and else [19,20].
  • 6. Nanomed. J., 3(1): 57-64, Winter 2016 62 Y. Yousefpoor et al. Fig. 2. Reduction of wounds area from 3.7 cm2 to zero on even days with trendlines 0.000 0.500 1.000 1.500 2.000 2.500 3.000 3.500 4.000 Day0 Day2 Day4 Day6 Day8 Day10 Day12 Day14 Control SNPs Alo SNPs-Alo Linear (Control) Linear (SNPs) Linear (Alo) Linear (SNPs-Alo) Fig. 3. Percentage of wound healing (PWH) from 0 to 100% on even days with trendlines 0 20 40 60 80 100 Day0 Day2 Day4 Day6 Day8 Day10 Day12 Day14 Control SNPs Alo SNPs-Alo Linear (Control) Linear (SNPs) Linear (Alo) Linear (SNPs-Alo) B2- Hemorrhage A2-Granulation tissue B1- Hemosiderin deposites A1-Fibrous tissue A2- Epithelialization C1-Complete Epithelialization C2- Fibrinoleukocytic exudate A1- Epithelialization B1- Granulation tissue Fig. 4. Optical Microscopy images of cells obtained from wounds and stained with Hematoxylin-Eosin
  • 7. Nanomed. J., 3(1): 57-64, Winter 2016 63 But it is certain that MBC test is done by the same mixed gel with connected particles. Result of this research shows that the Aloe vera gel accelerates wound healing, as in several studies have been investigated [21-24]. In several studies, good results have been taken from the SNPs along with other materials [7, 25-28]. However, this study shows that SNPs partly reduce rate of wound healing especially alone. It can be due to several effects of SNPs that interact with cells they are recovering. Asha Rani & et (2008) in a study on the toxicity of SNPs on the genome of human cells to conclude that SNPs enter to the cell and the nucleus and binding to the genetic material and they arrest cell cycle in the G2 phase of mitosis which can cause damage to cells, So it is possible that the lack of epithelialization in the SNPs (B) group is due to this action [29]. This means that toxicity effects of SNPs on the proliferation of epithelial cells in mitosis lead to the delayed recovery.According to Table 4, only complete epithelialization process can be observed in the control (A) and Aloe (C) groups, it is not formed in the SNPs (B) group and it was on average defective in the mixed (D) group. Chen et al [12] in 2008 in a study on the toxicity of SNPs concluded that SNPs cause a sharp decrease in mitochondrial activity and lead to cell malfunction. It has been found that silver ions seems to perturb mitochondria through interactions with thiol groups of the mitochondrial inner membrane.As these effects of silver ions could be completely blocked by sulfhydryl reagents, (e.g. reduced glutathione (GSH)), the ûndings clearly suggested that mitochondria were under oxidative stress when the cells were exposed to silver ions [12]. In conclusion, a preliminary outcome of this study could be that SNPs may interact with proteins and enzymes containing thiol groups such as glutathione, thioredoxin, SOD and thioredoxin peroxidase, are key components of the cell’s antioxidant defense mechanism and are responsible for neutralizing the oxidative stress of ROS largely generated by mitochondrial energy metabolism. SNPs may deplete the antioxidant defense mechanism which leads to ROS accumulationAccumulation of ROS could initiate perturbation and destruction of the mitochondria as shown in Table 4 [12, 30]. According to the investigated subjects, SNPs do not appear to increase wound healing as obtained in this study. In fact, it could be suggested that SNPs have delayed wound healing process. In the case of epithelialization defects in group treated with SNPs-Alo mixture, it could be suggested that the Aloe vera gel increased the rate of wound healing whereas SNPs decrease it, but the mixture of SNPs and Aloe gel has produced an effect which was the sum of each component of the mixture as shown in Figs 2 and 3. Perhaps the mixed gel had no effect on recovery, however, it is recommended for cases such as topical use in wound with severe infection, in patients with immunodeficiency who have wound or want to prevent ulcer formation such as Diabetic Foot, drug resistances and development of potential anti-bacterial biofilm for various biomedical and environmental applications against MRSA and MRSE[26]. CONCLUSION It could be concluded thatAloe vera gel is effective in speeding up the wound healing process but when mixed with SNPs, no significant improvement was observed in the healing rate. ACKNOWLEDGEMENTS We would like to extend our sincere thanks to those who collaborated including Prof. Ahmadian & Mrs Shafiizadeh of IBB Research Institute of Tehran University. Mr Ehsan Ghoddousi of Medicinal Plants Investigations Center of Jahad University of Kashmar for providing Aloe vera plant. We also appreciate Mr Javad Akhtari and Mrs Fatemeh Gheybi at BuAli Research Institute and Mrs Maasome Mazandarani at Dr. Shakeri PathobiologyLaboratory. The current study was derived from an MSc thesis. REFERENCES [1] Cotran RS, Kumar V, Collins T, Robbins SL. Robbins pathologic basis of disease: Saunders; 1999. [2] RAJAN S. Skin and soft-tissue infections: Classifying and treating a spectrum. Cleve Clin J Med. 2012; 79(1): 57- 66. [3] Zetola N, Francis JS, Nuermberger EL, Bishai WR. Community-acquired meticillin-resistant Staphylococcus aureus: an emerging threat. Lancet Infect Dis. 2005; 5(5): 275-86. [4] Sharrif Moghaddasi M. Aloe vera Chemicals and Usages. Advances in Environmental Biology. 2010; 4(3): 464-8. [5] Sharrif Moghaddasi M, Res M. Aloe vera their chemicals composition and applications: a review. Int J Biol Med Res. 2011; 2(1): 466-71. [6] Kumar KS, Bhowmik D, Biswajit C. Aloe vera: a potential herb and its medicinal importance. J Chem Pharm Res. 2010; 2: 21-9.
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