The Effects of Red Fruit (Pandanus Conoideus Lam)

Supplementation on Total Antioxidant Capacity and Creatine Kinase

in Rats after Maximal Physical Activity

Fajar Apollo Sinaga

, Pangondian Hotliber Purba

, Rika Nailuvar Sinaga

, Ramlan Silaban

Faculty of Sports Sciences, Universitas Negeri Medan, Medan, Indonesia

Department of Chemistry, Faculty of Mathematics and Natural Sciences, Universitas Negeri Medan, Indonesia

Keywords: Red fruit oil, Malondialdehyde, Total antioxidant capacity, Maximal physical activity, Antioxidant

Abstract: Maximal physical activity can produce an imbalance between ROS and antioxidants and thus may cause

oxidative stress and muscle damage which is possibly related to fatigue and tissue injury. Red fruit oil

(RFO) contains high beta-carotene and tocopherol as antioxidants which could overcome oxidative stress

condition. This study investigated the effect of RFO on total antioxidant capacity (TAC) and creatine kinase

(CK) after maximal physical activity. Forty rats were divided into 4 groups. The control group (I) was

administered with 1.5 ml distilled water, intervention groups (II), (III) and (IV) were administered with

different doses of RFO (0.15 ml/kgBW, 0.3 ml/kgBW, and 0.6 ml/kgBW, respectively). All groups were

trained to swim for 4 weeks and then were forced to swim without a load until being exhausted. The TAC,

CK levels and time of swimming to exhaustion were measured in all groups. The results showed that the

obtained CK level decreased significantly (P<0.05), TAC and time of swimming increased significantly (P<

0.05) in the intervention groups. The results suggest that red fruit oil can obviously reduce CK level,

increased TAC and endurance; it can also delay fatigue which is induced by maximal physical activity in the

rats.

1 INTRODUCTION

Skeletal muscle is a highly specialized tissue with

excellent plasticity in response to external stimuli

such as exercise and training. The repetitive muscle

contractions conducted during endurance training

lead to a variety of phenotypic and physiological

responses. These responses include activation of

mitochondrial biogenesis, fiber type transformation

and angiogenesis. Together, they increase the

muscle’s capacity of aerobic metabolism and its

resistance to fatigue. High muscle activity also

involves a strong increase in reactive oxygen species

(ROS) production (Steinbacher, and Eckl, 2015).

Accumulation of free radicals such as reactive

oxygen species (ROS) can cause damage to many

parts of the cells such as proteins, DNA, and cell

membranes by stealing their electrons via a process

called oxidation (Powers et al., 2011). The release of

ROS could result in lipid peroxidation in the

mitochondrial membrane. Damaged mitochondria

were found to reduce cellular respiration and

adenosine triphosphate (ATP) generation; they are

also among the primary causes of fatigue (Broome1

et al., 2018). Malondialdehyde (MDA) is one of the

results of lipid peroxidation induced by free radicals

during maximum physical exercise or high-intensity

endurance training (Yan and Hao, 2016; Lamou et

al., 2016), so MDA is a general indicator used to

determine the number of free radicals and indirectly

assess the body's oxidant capacity (Teng and Wu,

2017).

Several studies claim that oxidative stress can

lead to a decrease in the amount of antioxidants

including superoxide dismutase (SOD), catalase

(CAT), glutathione peroxide (GPx) and glutathione-

s-transferase (Thirumalai et al., 2011; Bulduk et al.,

2011), damages on the muscle tissue which is

thought to be involved in the process of fatigue,

causing muscle pain (Wan et al., 2017), with

indicators of increased levels of creatine kinase and

lactate dehydrogenase (Callegari et al., 2017),

changes in the value of hematocrit, erythrocytes,

316

Sinaga, F., Purba, P., Sinaga, R. and Silaban, R.

The Effects of Red Fruit (Pandanus Conoideus Lam) Supplementation on Total Antioxidant Capacity and Creatine Kinase in Rats after Maximal Physical Activity.

DOI: 10.5220/0009785503160322

In Proceedings of the 3rd Yogyakarta Inter national Seminar on Health, Physical Education, and Sport Science in conjunction with the 2nd Conference on Interdisciplinary Approach in Sports

(YISHPESS and CoIS 2019), pages 316-322

ISBN: 978-989-758-457-2

leukocytes (Senturk et al., 2004), decreased

hemoglobin levels and morphological changes in the

cells of erythrocytes (Senturk et al., 2005), which in

turn can affect performance. It is known, creatine

kinase (CK) is one indicator of the occurrence of

damage from muscle cells (Nogueira et al., 2019).

Naturally, the body has a defense mechanism

against ROS by an endogenous antioxidant system

which consists of superoxide dismutase (SOD),

glutathione peroxidase (GPx), and catalase (CAT)

(Ighodaro et al., 2018). This enzyme plays an

important role as a first-line protection against the

harmful effects of ROS generated by various

sources. However, when the production of ROS is

excessive, the function of endogenous antioxidant

will be limited. Therefore, the supplementation of

exogenous antioxidant from diet becomes important

to protect cells against the deleterious effect of ROS

(Hao, 2014). The results of several studies reported

that the administration of antioxidants derived from

natural or synthetic products from outside the body

is required to neutralize the free radicals formed

during physical activity, especially strenuous

physical activity (Teng and Wu, 2017; Xua et al.,

2017; Kalpana, 2012).

One of the known natural sources of antioxidants

is red fruit (Pandanus conoideus Lam) grown in

Papua. Research on the content of active compounds

in red fruit oil which has medicinal properties has

been carried out and was originally intended to

reveal its nutritional content. Red fruit oil contains

beneficial nutrients or high levels of active

compounds, including beta-carotene, tocopherol, and

fatty acids such as oleic acid, linoleic acid, linolenic

acid, and decanoic acid (Budi, 2005; Alamsyah,

2005). Tocopherol and beta-carotene are active

antioxidants believed to be potential on its ability to

prevent degenerative and chronic diseases such as

cardiovascular disease, atherosclerosis, and cancer.

In addition, the Papuan people believe that red fruit

can improve physical performance, but it still needs

to be proven scientifically.

The purpose of this study was to determine the

antioxidant effect of red fruit oil on total antioxidant

capacity (TAC) and creatine kinase (CK) after

maximal physical activity. The results are expected

to contribute to the development of science and

technology, especially as a basis for further research

and development phytopharmaca for the

improvement of public health, especially for the

health of athletes. The results could be applied to

athletes during training programs or during the

competition so as to support program development,

especially the development in the field of sports

achievement and health. In terms of the development

of science and technology, this research is a form of

contribution to disciplines other than sports

disciplines to support the athlete's performance.

2 MATERIALS AND METHODS

2.1 Tools

The tools used in this research were laboratory

glassware, vortex (Thermo), test tube (Iwaki),

Beckman coulter (Beckman), link Dako epitope

retrieval (Dako), tissue processor (Leica),

spectrophotometer (Shimadzu), analytical balance

(Boeco), syringe for oral feeding, flask 10 ml,

stopwatch, hairdryer, animal box, syringe 1 ml,

funnel, pipette, parchament, spatula, thermometer,

air pump and ruler.

2.2 Animal

Male rats of Wistar strain weighing 200-220 g were

obtained from the Animal House Faculty of

Pharmacy, University of Sumatera Utara. They were

placed in plastic cages in a room under standard

laboratory conditions (temperature 20 to 30

relative air humidity 45 to 55%, and 12/12 h

light/dark cycle). The rats were fed with a basal diet

and water ad libitum. All animal experiments

conducted during the present study got prior

permission from Institutional Animal Ethics

Committee, Department of Biology, Faculty of

Mathematics and Science, University of Sumatera

Utara.

2.3 Materials

Red fruit oil was taken from Papua, Indonesia.

Commercial assay kits for the detection of total

antioxidant capacity (TAC) and creatine kinase (CK)

were bought from Shanghai Korain Biotech Co., Ltd

(Shanghai, China). All other chemicals used were of

analytical grade and purchased from local suppliers.

2.4 Experimental Design

This study used 40 healthy male rats. The rats were

divided into four groups randomly consisted of ten

rats in each group. The control group (I) was

administered with 1.5 ml of distilled water,

intervention groups (II), (III) and (IV) were

administered with different doses of Red Fruit Oil

(0.15 ml/kgBW, 0.3 ml/kgBW, and 0.6 ml/kgBW,

respectively), per day using gavage spuit, for 28

days. The rats were trained to swim for a month, 30

The Effects of Red Fruit (Pandanus Conoideus Lam) Supplementation on Total Antioxidant Capacity and Creatine Kinase in Rats after

Maximal Physical Activity

317

min/day in the 1

week, 35 min/day in the 2

week,

40 min/day in the 3

week, and 45 min/day in the 4

week. After 28 days, the rats were forced to perform

the maximal activity by putting the rats in water with

no exit. The apparatus used was an acrylic plastic

pool (60, 50, and 50 cm in length, width, and height,

respectively) filled with fresh water, which was

maintained at 25 ± 0.5 °C at a depth of 40 cm.

Exhaustion was determined by observing the loss of

coordinated movements and failure to return to the

surface within 10 seconds. The exhaustive

swimming time was used as an indicator of exercise

endurance and anti-fatigue effects. Blood samples

were collected immediately after the exhaustive

exercise, and then TAC; CK levels were measured

using spectrophotometry.

2.5 Biochemical Assay

Blood sample (3ml) was collected into a plain tube

and allowed to clot for 45 min at room temperature.

Serum was separated by centrifugation at 2500 rpm

at 30°C for 15 min and utilized for the estimation of

various biochemical parameters, namely, total

antioxidant capacity (TAC) and creatine kinase

(CK). TAC and CK were analyzed by using a

creatine kinase and total antioxidant capacity assay

kit according to the manufacturer’s instruction.

2.6 Statistical Analysis

Data of research were tested for homogeneity and

normality to determine the type of statistics to be

used. Data were analyzed using one-way ANOVA

test to determine the mean difference between

treatments using SPPS 25.0 program. If there is a

significant difference, further proceed with the

Tukey test to determine the differences value

between treatment groups. Based on the significance

value, p<0.05 is considered statistically significant.

3 RESULTS AND DISCUSSION

3.1 Result

3.1.1 Effect of Red Fruit Oil on Creatine

Kinase Level

Based on the results of the analysis, it was found that

the mean level of creatine kinase (CK) in group I, II,

and III were 227.84±2.26, 203.77±1.94,

166.74±1.56; 129.29±1.62 U/L, respectively. The

normality and homogenous tests showed that the

data were normally and homogeneously distributed

(p>0.01). Meaning analysis using One Way

ANOVA test showed that the mean CK levels in the

four groups were significantly different (p <0.01).

Figure 1: Effect of Red Fruit Oil on Creatine Kinase (CK)

levels in serum of rats. Different letters indicate significant

difference at p < 0.05 by one-way ANOVA

As shown in Fig. 1, the creatine kinase (CK)

level of the II, III, and IV groups were significantly

lower than that of the I group (p < 0.01). The level

decreased level of creatine kinase was 10.57, 26.81

and 43.25% respectively.

3.1.2 Effect of Red Fruit Oil on Total

Antioxidant Capacity Level

Based on the results of the analysis, it was found that

the mean level of total antioxidant capacity (TAC) in

group I, II, III and IV were 1.54±0.04, 2.34±0.02,

2.64±0.03; 3.25±0.03 U/ml, respectively. The

normality and homogenous tests showed that the

data were normally and homogeneously distributed

(p>0.05).

Figure 2: Effect of Red Fruit Oil on Total Antioxidant

Capacity (TAC) levels in serum of rats

Meaning analysis using One Way ANOVA test

showed that the mean scores of TAC in the four

CK(U/L)

GROUP

YISHPESS and CoIS 2019 - The 3rd Yogyakarta International Seminar on Health, Physical Education, and Sport Science (YISHPESS

2019) in conjunction with The 2nd Conference on Interdisciplinary Approach in Sports (CoIS 2019)

318

groups were significantly different (p <0.05). As

shown in Fig. 2, the total antioxidant capacity (TAC)

levels of the group II, III, and IV were significantly

higher than that of the group I (p < 0.01). The

increased Total Antioxidant Capacity (TAC) levels

were 34.02, 109.30 and 100.17% respectively.

3.1.3 Effect of Red Fruit Oil on Swimming

Time to Exhaustion of Rats

As shown in Fig. 3, the exhaustive swimming times

in the group II, III, and IV (65.83 ±1.47, 76.50

±1.05, and 107.5 ± 1.87 min, respectively) were

significantly higher than that in the group I (44.00 ±

1.41 min) (p < 0.01). Swimming time increased were

49.61, 73.86 and 144.31% respectively. These

results suggest that red fruit oil have anti-fatigue

activity and could enhance exercise endurance.

Figure 3: Effects of red fruit oil on swimming time

to exhaustion of rats. Different letters indicate

significant difference at p < 0.05 by one-way

ANOVA

3.2 Discussion

It is known that physical activity can increase the

production of various types of free radicals which

can damage cell membranes, skeletal muscle

performance, macromolecule and cellular function

impairment (Simioni et al., 2018). Free radicals

formed in the body will be neutralized by the body's

defense systems such as antioxidants enzymes such

as catalase (CAT), superoxid dismutase (SOD),

glutathione peroxidase (GPx), and a number of non-

enzyme antioxidants such as vitamin A, E and C,

glutathione, ubiquinone, and flavonoids (Rao et al.,

2011). When the production of free radicals exceeds

cellular defense antioxidants, oxidative stress will

occur (Kawamura and Muraoka, 2018). Oxidative

stress has been identified as one of the factors

leading to fatigue (Theofilidis et al., 2018).

In this study, the administration of red fruit oil in

mice who got training for one month could increase

total capacity antioxidants, time of swimming and

reduce creatine kinase levels when the rats carried

out maximum physical activity. This result was due

to the antioxidants in red fruit oil that neutralize or

scavenge the free radicals. Red fruit oil contains

beneficial nutrients or bioactive compounds at high

levels, such as beta-carotene, tocopherol, as well as

fatty acids (Budi, 2005; Roreng et al., 2014).

Carotenoids (e.g. β-carotenes) lipid-soluble

antioxidants located primarily in biological

membranes, could reduce lipid peroxidation; studies

show that astaxanthin, a member of the carotenoid

family, and a dark-red pigment found in the marine

world of algae and aquatic animals such as salmon,

red sea bream as well as in birds such as flamingo

and quail, have potential health-promoting effects in

the exercise-induced fatigue (Dhankhar et al., 2012).

A research conducted by Rohman et al. reported that

red fruit has antioxidant activity that can be used as

free radical scavengers. Rohman et al. reported in

vitro study showed that the red fruit oil exhibited

antioxidant activity with IC50 of 451.51 μg/ml. In

vivo study, red fruit oil with a dosage of 0.15, 0.3,

and 0.6 mg/kg BW exhibited the ability to lower the

blood MDA level (Rohman et al., 2010). The result

of this research is in line with the research conducted

by Sandhiutami et al. which studied the level of

tocopherol after red fruit oil supplementation on

male Wistar rats at the maximal activity. They found

that the level of tocopherol increased as the dosage

of red fruit oil is risen (Sandhiutami et al., 2012).

This study also found that the administration of

red fruit oil could increase total antioxidant capacity

(TAC) and reduce creatine kinase levels. The

increased total antioxidant capacity (TAC) and

reduced creatine kinase levels was due to the high

antioxidant content in red fruit oil such as

carotenoids (11.500 ppm), β-carotene (694.80 ppm),

tocopherols (11.200 ppm), and α-tocopherol (495.50

ppm) (Roreng et al., 2014). The increased

antioxidant total antioxidant capacity (TAC) is

supported by the results of research conducted by

several researchers. Derami and Roohi (2019)

reported that the administration of omega-3 fatty

acid for in nonathlete young males after four weeks

of endurance exercise could increase total

antioxidant activity (Derami and Roohi, 2019).

Omega 3 is a rich source of antioxidants, such as

marine carotenoids (for example astaxanthin and

fucoxanthin), vitamins A and E, and phospholipids

containing long-chain n-3 e polyunsaturated fatty

acids (PUFAs) (Gammone et al., 2019). Poulab et al.

reported the effect of a four-week acute vitamin C

supplementation on the markers of oxidative stress

and inflammation following eccentric exercise in

The Effects of Red Fruit (Pandanus Conoideus Lam) Supplementation on Total Antioxidant Capacity and Creatine Kinase in Rats after

Maximal Physical Activity

319

active men can significantly increase total

antioxidant capacity (0.19 mm/l) and reduce creatine

kinase levels (Poulab et al., 2015). Taghiyar et al.

reported the results of his research that supplements

of vitamins C and E play a role in reducing the

marker of muscle damage in aerobic exercise

characterized by the reduction of creatine kinase

levels (Taghiyar et al., 2013). Dehghan et al.

reported that additional use of regular training and

cinnamon bark extract (CBE) supplementation

increase TAC and protect healthy male rats against

oxidative damage induced by exhaustive exercise

(Dehghan et al., 2015).

The results of this study showed that red fruit oil

was able to elevate the rat endurance. This effect

was indicated by the longer swimming time in all

treatment groups compared to the control group.

Statistical analysis showed that the higher red fruit

oil dose resulted in a longer swimming time. Several

theories support this result, namely because of the

high antioxidant content in red fruit oil. Antioxidants

in red fruit oil were expected to prevent lipid

oxidation in cellular membrane especially in

erythrocyte cells. Some research showed that

physical activities are able to induce the formation

of oxidized lipid and generate the oxidative stress

condition. Oxidized lipids can be the cause of

erythrocyte cell damage and thus cause the "sport

anemia" (Marjan Wouthuyzen-Bakker and Sander

van Assen, 2015; Sinaga, 2017) and muscle tissues

damage (Sinaga and Purba, 2018). The damage of

muscle and blood cells are considered to be involved

in exhaustion processes or the disability to generate

energy and therefore decrease the endurance. The

increased swimming time due to administration of

antioxidants in all treatment groups compared to the

control group was supported by the results of

research conducted by several researchers. Xianchu

et al. reported that treatment of grape seed

proanthocyanidin extract (GSPE) at a dose of 50 and

100 mg/kg/day of body weight significantly relieved

exhaustive exercise-induced fatigue, which was

indicated by the increasing forced swimming time.

In addition, the treatment of GSPE significantly

improved the creatine phosphokinase and lactic

dehydrogenase, as well as lactic acid level in

exhaustive swimming. For underlying mechanisms,

treatment of GSPE had anti-fatigue effects by

promoting antioxidant ability and resisting oxidative

effect, as represented by increased total antioxidative

capability levels, enhanced superoxide dismutase

and catalase activities, and ameliorated

malondialdehyde levels (Xianchu et al., 2018). A

study about the effect of antioxidant on the

endurance has been conducted and it reported that

vitamin C was also able to increase endurance in the

rat model (Ozaslan et al., 2004). Lamou et al.

reported that the leaf aqueous extract of M. Oleifera

possesses anti-fatigue properties. It improved the

swimming ability of rats by delaying the

accumulation of blood lactate and blood urea

nitrogen, by increasing the mobilization and the use

of body fats and by slowing the depletion of

glycogen stores. The anti-fatigue potential may be

expressed through mechanisms that involve the

antioxidant activity of the extract (Lamou et al.,

2016). Xu and Wang reported that flavonoids from

Lotus (Nelumbo nuficera Gaertn) leaf (FFL) can

extend the exhaustive swimming time of the mice, as

well as increase the superoxide dismutase (SOD),

glutathione peroxidase (GSH-Px) activities, but

decrease the malondialdehyde (MDA) and 8-

hydroxy-2′-deoxyguanosine (8-OHdG) levels. These

results indicated that FLL possessed protective

effects against exhaustive swimming exercise-

induced oxidative stress (Xu and Wang, 2018). Bing

and Wang reported that Ginkgo biloba extract was

able to increase the activities of antioxidant enzymes

in rat liver tissues, reduce the level of oxidized lipid

generated by free radicals and increase endurance

and healing processes after maximal physical

activities (Bing and Wang, 2010). A similar result

was also reported by Miao et al using corn peptide

(Miao et al., 2010).

4 CONCLUSIONS

It can be concluded from the present study that red

fruit oil has endurance and delay fatigue induced by

maximal physical activity in rat, and its anti-fatigue

mechanisms that involve the following protects

exercise-induced oxidative stress by increasing the

levels of TAC, as well as decreasing the CK levels

of rats.

ACKNOWLEDGEMENTS

The authors thank Directorate for Higher Education,

The National Education Ministry of Republic

Indonesia for Research Grant of Hibah Fundamental

for financial support.

YISHPESS and CoIS 2019 - The 3rd Yogyakarta International Seminar on Health, Physical Education, and Sport Science (YISHPESS

2019) in conjunction with The 2nd Conference on Interdisciplinary Approach in Sports (CoIS 2019)

320

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