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International Journal of Pharma Medicine andBiological Sciences

IJPMBS is a scholarly peer-reviewed international scientific journal published

quarterly, focusing on theories, systems, methods, algorithms and applications in

Pharma Medicine and Biological Sciences. It provides a high profile, leading edge

forum for academic researchers, industrial professionals, engineers, consultants,

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2016

ISSN: 2278-5221

Editor-in-Chief: Dr. Vasudeo Zambare

DOI: 10.18178/ijpmbs

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It's a great honor for me to serve as the editor-in-chief of

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and hopefully it will become a recognized journal

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Elemental Research for Quantification of Eustachian Tube

Insufflation Method

Yutaka Suzuki, Osamu Sakata, Shun’ichi Imamura, Shuichiro Endo,

Akihito Mizukoshi, Asobu Hattori, and Masayuki Morisawa

Commercial equipment is available for conducting Eustachian tube

function tests but, generally, the Eustachian tube insufflation method

doubles as a treatment and diagnosis. However, with the Eustachian

tube insufflation method, the doctor merely performs...[Read more]

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8/6/2016 Lower Ratio of Collagen’s Fibre Type III/Type I and Higher Tensile Strength in Injured Rabbit’s Achilles Tendon Treated with Astaxanthin - Volume 5, No. 2,…

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Home > Published Issues > 2016 > Volume 5, No. 2, April 2016 >

Lower Ratio of Collagen’s Fibre Type III/Type I and Higher Tensile Strength

in Injured Rabbit’s Achilles Tendon Treated with Astaxanthin

Krisna Saputra I. Komang Agus 1, Astawa I. Putu 1, Mulyadi Ridia K. G. 1, and Nindhia Tjokorda Gde Tirta 2

1. Program Studies of Orthopaedic Surgery and Traumatology, Medical Faculty of Udayana University, Denpasar, Indonesia

2. Material Engineering Division, Department of Mechanical Engineering, Engineering Faculty of Udayana University, Denpasar, Indonesia

Abstract—Tendon injuries vary from minor to total tear that requires surgery. The mechanical disturbance

is the most complication. Inflammatory process and formation of free radicals can worsen tendon healing.

Astaxanthin can be used to help tendon healing. This study aims to prove ratio of collagen type III/type I

was lower and the tensile strength was higher on the administration of astaxanthin. This study is an

experimental research using post-test only control group design with rabbit as subject. A total of 32

research subjects which meet inclusion were randomly divided into treatment and control groups. The

treatment group is the group that was given astaxanthin after Achilles tendon was sharply cut and sewn,

while the control group was not given astaxanthin. Statistical analysis using independent t-test found

significant difference between treatment and control groups. The ratio of collagen type III/type I of the

rabbit Achilles tendon which receive treatment of astaxanthin is smaller than the untreated group p =

0.000 (p<0.05). The tensile strength is greater in treatment group than the non-treated group with p =

0.044 (p<0.05). The result showed that the ratio of collagen type III/type I was lower when treated with

astaxanthin thus can help improve the tensile strength.

Index Terms—Astaxanthin, rabbit’s Achilles tendon injuries, ratio of collagen type III/I, tensile strength

Cite: Krisna Saputra I. Komang Agus, Astawa I. Putu, Mulyadi Ridia K. G., and Nindhia Tjokorda Gde

Tirta, "Lower Ratio of Collagen’s Fibre Type III/Type I and Higher Tensile Strength in Injured Rabbit’s

Achilles Tendon Treated with Astaxanthin," International Journal of Pharma Medicine and Biological

Sciences, Vol. 5, No. 2, pp. 121-124, April 2016. 10.18178/ijpmbs.5.2.121-124

Previous paper Elemental Research for Quantification of Eustachian Tube Insufflation Method

Next paper A New Direction of Cancer Treatment through the Development of the Anti-Oxidant Function

of Hydrogen Water


8/88 6/66 2016 Lowoo er Ratio ofo Collagen’s Fibre TyTT pe III/T// yTT pe I and Higher TeTT nsile Strength in Injn ured Rabbit’s AcAA hilles TeTT ndon Treated with AsAA taxaa anthin - VoVV lume 5, No. 2,…

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Home > Published Issues > 2016 > Volume 5, No. 2, April 2016 >

Article# Article Title & Authors (Volume 5, No. 2, April 2016) Page

1The Coupling of the IoT in the Era of Big Data and the CTC Test Detecting miRNA with Using a

Molecular Torch Technique

Jiyun Kim

99

2Towards Early Detection of Diabetic Retinopathy Using Extended Fuzzy Logic

Mohammed Imran, Alhanouf M. Al-Abdullatif, Bushra S. Al-Awwad, Mzoon M. Alwalmani, Sarah A. Al-

Suhaibani, and Shahad A. Al-Sayah

110

3Elemental Research for Quantification of Eustachian Tube Insufflation Method

Yutaka Suzuki, Osamu Sakata, Shun’ichi Imamura, Shuichiro Endo, Akihito Mizukoshi, Asobu Hattori,

and Masayuki Morisawa

115

4Lower Ratio of Collagen’s Fibre Type III/Type I and Higher Tensile Strength in Injured Rabbit’s Achilles

Tendon Treated with Astaxanthin

Krisna Saputra I. Komang Agus, Astawa I. Putu, Mulyadi Ridia K. G., and Nindhia Tjokorda Gde Tirta

121

5A New Direction of Cancer Treatment through the Development of the Anti-Oxidant Function of

Hydrogen Water

Jiyun Kim

125

6In Vitro Synergistic Effects of Snail Slime and Chitosan against Staphylococcus aureus

Agnes Sri Harti, Estuningsih, Heni Nur Kusumawati, Siswiyanti, and Arum Setyaningtyas137

7The Synergistic Effects of Areca Nut Extract and Chitosan toward Candida albicans in Vitro

Rahajeng Putriningrum, Anis Nurhidayati, Tresia Umarianti, Kartika Dian Listyaningsih, and Wahyu

Rima Agustin

142


8/88 6/66 2016 VoVV lume 5, No. 2, April 2016 - IJPMBS




Lower Ratio of Collagen’s Fibre Type III/Type I

and Higher Tensile Strength in Injured Rabbit’s

Achilles Tendon Treated with Astaxanthin

Krisna Saputra I. Komang Agus, Astawa I. Putu, and Mulyadi Ridia K. G. Program Studies of Orthopaedic Surgery and Traumatology, Medical Faculty of Udayana University, Denpasar,

Indonesia

Email: [email protected], {putu_astawa, mulyadi_ridia}@yahoo.com

Nindhia Tjokorda Gde Tirta Material Engineering Division, Department of Mechanical Engineering, Engineering Faculty of Udayana University,

Denpasar, Indonesia

Email: [email protected]

Abstract—Tendon injuries vary from minor to total tear

that requires surgery. The mechanical disturbance is the

most complication. Inflammatory process and formation of

free radicals can worsen tendon healing. Astaxanthin can be

used to help tendon healing. This study aims to prove ratio

of collagen type III/type I was lower and the tensile strength

was higher on the administration of astaxanthin. This study

is an experimental research using post-test only control

group design with rabbit as subject. A total of 32 research

subjects which meet inclusion were randomly divided into

treatment and control groups. The treatment group is the

group that was given astaxanthin after Achilles tendon was

sharply cut and sewn, while the control group was not given

astaxanthin. Statistical analysis using independent t-test

found significant difference between treatment and control

groups. The ratio of collagen type III/type I of the rabbit

Achilles tendon which receive treatment of astaxanthin is

smaller than the untreated group p = 0.000 (p<0.05). The

tensile strength is greater in treatment group than the non-

treated group with p = 0.044 (p<0.05). The result showed

that the ratio of collagen type III/type I was lower when

treated with astaxanthin thus can help improve the tensile

strength.

Index Terms—Astaxanthin, rabbit’s Achilles tendon injuries,

ratio of collagen type III/I, tensile strength

I. INTRODUCTION

Tendon as an organ which connects muscle to bone

and enable power transmission generated by the muscle

to the bone resulting in movement of the joint. Most

tendon injuries occur in areas near the joints, such as

shoulders, elbows, knees, and ankles. Injury to the joints

accompanied by partial or total tear of the tendon occurs

as much as 45% of all musculoskeletal injuries each year.

[1], [2] Injuries to the tendon are quite often, occurs in

30% - 50% of all injuries. These injuries mainly occur

due to accidents, traffic accidents or sports injuries [3].

Manuscript received April 27, 2016; revised June 2, 2016.

Complications that often occur as a result of this

tendon injuries are disruption of flexibility, stiffness and

reduced strength of the tendon itself. Thus the function of

a tendon as a buffer as well as the nature viscoelasticity to

reduce muscle damage will be decreased so that the

movement and function of protection are limited [1], [3],

[4]. The main purpose of tendon healing is to restore the

mechanical properties of the tendon (gliding function).

Tendons have a poor spontaneous regenerative capacity

after injury, so that the pre injury biological and

biomechanical function are hard to achieve [4]. This is

due to the formation of adhesions and scar tissue which

inhibit the regenerative process of the tendon.

In the process of tendon healing, change in the type

and distribution of collagen tissue occur. Increase in ratio

of collagen type III/I. The synthesis of type I collagen in

tendon injury grade III will decline and will be replaced

by increase in the synthesis of collagen type III in line

with the expansion of granulation tissue and remodelling

process so that the ratio of collagen type III/I increases

and substituted by scar tissue and fibrosis. The formation

of scar tissue in the tendon can cause adhesion and

decrease of tensile strength up to 20% [5]-[7].

In the phase of healing tendon, many hormones and

molecules that come into play. Injuries that occur in the

tendon can trigger the formation of free radicals such as

hydrogen peroxide and release of inflammatory mediators

such as TNF-a, IL-1, IL-6 and IL-10. The free radicals

can activate metalloproteinase enzymes, and increased

the expression of PGE2 which degrade tendon collagen

matrix. This inflammatory process can also trigger the

release of growth factors such as TGF-b which induce a

dramatic tenocyte and fibroblast infiltration, causing

extensive reorganization of collagen. The proportion of

type III collagen formation is higher than type I due to the

inhibitory effect of PGE-2 on the synthesis of collagen I

mRNA and increased expression of collagen type III [8]. Various methods have been carried out to restore the

function of the tendon after injury. The choice of therapy

International Journal of Pharma Medicine and Biological Sciences Vol. 5, No. 2, April 2016

©2016 Int. J. Pharm. Med. Biol. Sci. 121

doi: 10.18178/ijpmbs.5.2.121-124

can be non-operative and operative with or without graft

followed by immobilization or controlled mobilization.

Some of these methods fail to regain normal function

after injury, so that the researchers focused on the quality

of therapeutic modalities and acceleration of tendon

healing after injury. Modalities developed include usage

of growth factors or substances that can affect the

expression of growth factors, genes transfer or cell

therapies [8], [9]. Antioxidant supplementation is one of

the agents that have strong anti-inflammatory abilities,

useful in healing process of tendon injuries.

Oxidative stress can interfere with the healing process.

Fibroblasts tendon will form unorganized collagen

components. The proliferation of collagen type III will

increased, and the maturation of cross-linked collagen

fibres become slow. The collagen components will

become fibrotic, stiff, has a low modulus and uneven

distribution of load bearing [10], [11]. These events cause

a decrease in tendon mechanical components up to 45.2%,

making it vulnerable to rupture again [10], [11].

The use of potent antioxidants i.e. Astaxanthin in the

tendon injury may help reduce oxidative stress due to the

formation of ROS. It has a suppressive effect on the

expression of MMP, PGE2 as well as growth factors such

as TGF-β so that the fibrosis process in the healing of

tendon injuries can be reduced [8], [11]-[13].

II. MATERIALS AND METHODS

The experiment was conducted from December 2015

to January 2016 at the faculty of Veterinary Medicine

Udayana University Bali. The aim of this study is to

prove administration of Astaxanthin can reduce the ratio

of collagen fibres type III/I and increase tensile strength

of tendon healing. This study is an experimental research

design using post-test only control group design with the

subject rabbits from eligible subject population with

randomized sampling.

Sixteen adult male New-Zealand White rabbits of the

same age (12 weeks) weighing 2 – 3kg were used in this

experiment. All the animal was given adequate food and

water in the laboratory. These rabbits were divided

randomly into control and treatment groups. The control

group was not given Astaxanthin, while the treatment

group was given Astaxanthin after Achilles tendon had

been cut sharply and sewn with the non-absorbable nylon

thread (monofilament 4-0) with a 4 strand modified

Kessler technique. Followed with immobilization of the

affected limb with a cast.

The Astaxanthin was given 4mg (AstaREAL 200mg)

ad libitum with dose 0.106mg/kgbw/day for about 3

weeks. After that, the rabbits were sacrificed and the

Achilles tendon was isolated for further examination.

The rabbit tendon tissues were examined for tensile

strength in the vertical direction in which the tendon is

stretched until load failure with universal testing machine.

The immunohistochemistry examination is then

performed to know the ratio of collagen type III/I. This

procedure is carried out with rabbit tendon tissue fixation

using 10% neutral buffered formalin and processed for

routine histological preparations with anti-mouse

collagen III/I antibody and secondary antibody anti-

mouse IgG/biotin which has been conjugated with

horseradish peroxidase. The calculation of the amount of

collagen tendon using the Image J. Network processing.

The obtained data are presented as mean ± SD of

number of rabbits (n) used in the experiment. The mean

difference was analysed with independent t-test for

statistical significant of examined variables i.e. the tensile

strength and the ratio of collagen III/I. The difference was

assumed to be significant at p<0.05.

III. RESULTS

The distribution of the research subjects are as many as

32 subjects. The treatment group with the administration

of Astaxanthin is as much as 16 or 50.00% of the total

subjects and the control group without the administration

of Astaxanthin as many as 16 or 50.00%.

The mean of tensile strength in the treatment group

was 92.56 N ± 4.3384 while the average tensile strength

in the control group was 88.53 N ± 6.3248. The highest

tensile strength was 98.74 N ± 4.3385 in the treatment

group and the minimum tensile strength was 80.05 N ±

6.3248 found in the control group. The mean percentage

of type III collagen in the treatment group was 14.80% ±

2.0559, while the control group was 29.70% ± 6.4301.

The mean of collagen type I in the treatment group was

86.25% ± 0.9402, while in the control group was 73.07%

± 4.7582. The ratio of collagen III/I in the treatment

group was 0.172 ± 0.0242 compared with the control

group 0.408 ± 0.0919. The smallest ratio found in the

treatment group with ratio 0.133 ± 0.0242 while the

highest ratio found in the control group with ratio 0.570 ±

0.0919.

TABLE I. THE MEAN OF TENSILE STRENGTH AND COLLAGEN TYPE

III/I RATIO

Variables

Groups

Treatment with

Astaxanthin(n=16)

(Mean ± SD)

Control without

Astaxanthin(n=16)

(Mean ± SD)

Collagen Type III(%)

14,80 ± 2,0559 29,70 ± 6,4301

Collagen Type I

(%)86,25 ± 0,9402 73,07 ± 4,7582

Ratio of Collagen

III/I0,172 ± 0,0242 0,408 ± 0,0919

Tensile Strength (N)

92,56 ± 4,3384 88,53 ± 6,3248

Figure 1. Tensile strength distribution among groups



Table I and Fig. 1 showed that tensile strength is

higher in the treatment group compared with the control

group, and the mean difference between treatment and

control group was statistically significant with p=0.044

(p<0.05).

While the ratio of collagen type III/I in the treatment

group is smaller than the control group, and the mean

difference between treatment and control group was

statistically significant with p=0.000 (p<0.05) as seen on

Fig. 2.

Figure 2. The ratio of collagen type III/I distribution among groups

IV. DISCUSSION

A. Effects of Astaxanthin on the Ratio of Collagen III/I

The results of the study are consistent with previous

study by Bauge and Mizuta that mentioning the

proportion of type I collagen synthesis and expression

will be improved whereas the type III will be suppressed

so that the ratio of mRNA expression of collagen III/I

will fall in the injured tendon that supplemented with

antioxidants such as Astaxanthin and spirulina (TOL19-

001) [8], [11]. This is due to the activity of Astaxanthin

inhibits the formation of ROS, IL-1b and PGE2 so that

the inflammatory process can be less extensive and

apoptosis is inhibited. Another study by Kishimoto and

Song showed that Astaxanthin can inhibit several MMP

expression and performance including MMP-1, MMP-2,

MMP-8, MMP-13 and MMP-14 collagenase activity by

suppressing ROS generation and IL -1. This process will

prevent fibrogenesis and degradation of collagen fibrils

type I [14], [15]. The collagen fibrils type I on the

treatment group is thicker and regularly arranged as seen

on Fig. 3 compared with control, whereas the type III is

less composed than type I as seen on Fig. 4.

(a) (b)

Figure 3. The histopathology image of collagen type I of the Achilles tendon on the treatment group (a) compared with the control group (b)

(a) (b)

Figure 4. The histopathology image of collagen type III of the Achilles tendon on the treatment group (a) compared with the control group (b)

B. Effect of Astaxanthin on Tendon Tensile Strength

The results of the study are consistent with previous

research by Woo and Aro which demonstrated that

tendon with dominant composition of type I collagen

cross-link will increase its tensile properties [7], [9].

Antioxidants such as Spirulina (TOL19-001) can help

improve cross-linking, tensile strength, elasticity and

structure of the tendon [8]. Those findings were inline

with this study where the tensile strength of tendon in the

group treated with Astaxanthin was significantly higher

than the control group. The mean tensile strength tendon

after treatment is still in the normal range of tensile

strength in rabbits, but the maximum strength after

loading decreased compared with normal tendon. The

biomechanical component of tendon after a grade III

injury still inferior compared with normal tendon [7].

V. CONCLUSION

Our study investigated the effect of Astaxanthin as an

antioxidant on ratio of collagen type III/I and tensile

strength of Achilles tendon after injury. The results

showed that Astaxanthin significantly lowering the ratio

of collagen type III/I and thus increasing the tensile

strength. We suggest further experiment over the role of

antioxidant on musculoskeletal events.

ACKNOWLEDGMENT

The authors wish to thank the Orthopaedic and

Traumatology Department, Machinery Technical

Department and the Veterinary Department of Udayana

University for all the support and facilitations during the

research.

REFERENCES

[1] K. A. Hilderbrand, L. Corrie, G. Behm, Alison, and D. A. Hart, “The basic of soft tissue healing and general factors that influence

such healing,” Sports Med. Arthrosc. Rev., vol. 13, no. 3, pp. 136-144, 2005.

[2] S. P. Tendon, “Injury and tendinopathy: Healing and repair,” The

Journal of Bone and Joint Surgery, vol. 87, pp. 187-201, 2006. [3] T. Jarvinen, P. Kannus, and N. Mafulli, “Achilles tendon disorders

etiology and epidemiology,” Foot Ankle. Clin. N Am., vol. 10, pp. 255-266, 2005.

[4] S. Giannotti, et al., “Treatment of tendon injuries of the lower

limb with growth factors associated with autologous fibrin scaffold or collagenous scaffold,” Surg. Technol. Int., vol. 26, pp.

324-328, 2015.[5] N. Maffulli, P. Renstrom, and W. B. Leadbetter, “Tendon

injuries,” in Basic Science and Clinical Medicine, Springer-Verlag

London Limited, 2005, pp. 3-313.



[6] W. Romani, P. Langenberg, and S. M. Belkoff, “Sex, collagen expression, and anterior cruciate ligament strength in rats,”

Journal of Athletic Training, vol. 45, no. 1, pp. 22-48, 2010.

[7] S. L. Woo, T. M. Vogrin, and S. D. Abramowitch, “Healing and repair of ligament injuries in the knee,” J. Am. Acad. Orthop.

Surg., vol. 8, pp. 364-372, 2000.[8] C. Bauge, S. Leclercq, T. Conrozier, and K. Boumediene,

“TOL19-001 reduces inflammation and MMP expression in

monolayer cultures of tendon cells,” BMC Complementary and Alternative Medicine, vol. 15, p. 217, 2015.

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Krisna Saputra I Komang Agus was born in Semarapura, town of Bali on 1983. He

graduated from Medical Faculty of

Wijayakusuma University on 2010. He pursued his orthopaedic surgeon at the

Medical Faculty of Udayana University since 2011. Currently he is an orthopaedic registrar

at Sanglah hospital Denpasar Bali.

Astawa I Putu was born in Bangli, town of

Bali on 1953. He graduated from Medical Faculty of Udayana University in 1979. He

was devoting himself in the Department of Surgery Faculty of Medicine Udayana

University and continuing education in the

Specialist of Orthopaedic and Traumatology at Airlangga University, school of Medicine

which was completed in 1987.

He also later graduated at Sports Physiology Faculty of Medicine Udayana University and earned Master of Health in 1998. He received

Doctor degree the Faculty of Medicine Udayana in 2007 and was a full

professor in the field of Orthopaedic and Traumatology. He currently is the Dean of the Faculty of Medicine, University of Udayana.

Mulyadi Ridia K G was born in Negara, town of Bali on 1960. He graduated from

Medical Faculty of Udayana University on 1986. He continued his education

Orthopaedics and Traumatology at Airlangga

University School of Medicine and graduated in 1996. He had worked at North Wakarumba

and Guali Health Center as a Physicians from 1987 to 1989.

He devoted himself as the staff at

Orthopaedics and Traumatology Medical Faculty Udayana since 1997, then followed Spine fellowship training in 2002-2003 in Jakarta, New

York and Tokyo and reaching Brevet of Spine Consultant at the Faculty of Medicine, University of Indonesia in 2003.

Tjokorda Gde Tirta Nindhia was born in Denpasar, Bali, Indonesia on January 16th,

1972. Received Doctor Degree in Mechanical

Engineering from Gadjah Mada University (UGM) Yogyakarta, Indonesia on August

2003, with major field of study was Material Engineering. He participated in various

international research collaboration such as

with Muroran Institute of Technology Japan (2004), Toyohashi University of Technology

Japan (2006), Leoben Mining University Austria (2008-2009), Technical University of Vienna Austria (2010) and Recently with

Institute Chemical Technology of Prague Czech Republic (2012-now).

His current job is as Full Professor in the field of Material Engineering at Department of Mechanical Engineering, Engineering Faculty,

Udayana University, Jimbaran, Bali, Indonesia. His research interest covering subjects such as, biomaterial, waste recycle, failure analyses,

ceramic, metallurgy, composite, renewable energy, and environmental

friendly manufacturing. Prof. Nindhia is a member of JICA Alumni, ASEA-UNINET alumni, International Association of Computer Science

and Information Technology (IACSIT), Asia-Pacific Chemical, Biological & Environmental Engineering Society (APCBEES) and also

member of association of Indonesian Nanotechnology. Prof Nindhia

received best researcher award in 1997 and in 2013 from Udayana University the place where he is working and again in 2012 received

both Best lecturer award from Engineering Faculty of Udayana University. In the same years 2012, the research center of Udayana

University awarded Prof Nindhia as the best senior researcher. In 2013,

Prof. Nindhia awarded as 15 best performance Indonesian lecturers from Ministry of Education and Culture the Republic of Indonesia.

