The Effects of Administering Jicama Concentrate (Pachyrhizus
erosus) and Kefir Grains as a Synbiotic Drink on Malondialdehyde
and Superoxide Dismutase Levels in the Testicles of Hyperlipidemic
Rats
Mohammad Alvian Subhakti
1
a
, Miranti Dewi Pramaningtyas
1
b
, Rafik Prabowo
1
c
and Rokhima Lusiantari
1
d
1
Department of Physiology, Faculty of Medicine, Universitas Islam Indonesia, Yogyakarta, Indonesia
Keywords: Hyperlipidemia, Pachyrhizus erosus, Kefir, Malondialdehyde, Superoxide Dismutase
Abstract: Background: More than half of infertility prevalence come from men. There is a correlation between
hyperlipidemia and male infertility. Malondialdehyde (MDA) and superoxide dismutase (SOD) are oxidative
stress markers which indicate the testicular tissue damage caused by hyperlipidemia. The management of
hyperlipidemia continues to develop to date, and synbiotics are potential for hyperlipidemia therapy.
Objective: To examine the effects of jicama concentrate and kefir grains as a synbiotic drink on the levels of
MDA and SOD of the testicles in hyperlipidemic rats. Methods: Twenty-five male Wistar rats were divided
into 5 groups and given quail egg yolk for a month. The intervention group was given a synbiotic drink at a
dose of 5ml/200grBW for a month with different combinations of jicama concentrate and kefir. The levels of
MDA and SOD activity were checked after intervention. Result: The results showed that the mean MDA
levels (nmol/ml) were 12.30 ± 0.28 (K +), 2.83 ± 0.27 (K-), 8.43 ± 0.38 (P1), 6.34 ± 0.29 (P2), and 4.49 ±
0.25 (P3) while the mean SOD activities (%) were 32.86 ± 6.75 (K+), 82.14 ± 7.57 (K-), 43.21 ± 5.56 (P1),
62.14 ± 7.40 (P2), 70.35 ± 4.82 (P3). There were significant differences in the MDA levels among all groups
(p <0.01), whereas in SOD activities the differences were found among all groups except between K+ and P1,
K- and P3, as well as P2 and P3 (p> 0.05). Conclusion: Jicama concentrate and kefir grain as a synbiotic drink
significantly decrease MDA and increase SOD in testicular hyperlipidemic rats.
1 INTRODUCTION
Infertility becomes one of the health problems which
is estimated to keep increasing in the future. The high
rate of infertility is influenced by contamination from
the environment and lifestyle changes (Pushpendra &
Jain, 2015). The estimated infertility incidence in
productive age couples in the world is 8% to 12%,
with a global average of 9% (Inhorn & Patrizio,
2015). In fact, more than half of the infertility cases
in the world come from male partners (Pushpendra &
Jain, 2015). There are a number of both internal and
external factors which lead to the emergence of
infertility in men. Schisterman stated that there is a
a
https://orcid.org/0000-0003-4248-8393
b
https://orcid.org/0000-0003-1215-881X
c
https://orcid.org/0000-0003-0827-3591
d
https://orcid.org/0000-0002-3760-2553
correlation between high levels of blood lipids or
hyperlipidemia and infertility in men. The
concentration of lipids has an effect on semen
parameters, especially on the morphological changes
in the head of the sperm which affects male fertility
(Schisterman et al., 2014).
Hyperlipidemia is an abnormal condition in lipid
metabolism which is characterized by an increase in
the lipid fractions. Changes in lipid fractions include
increased cholesterol and triglyceride levels in the
blood to above the normal values (Nirosha et al.,
2014). Hypercholesterolemic conditions can damage
various organs in the human body (Pushpendra &
Jain, 2015), including the heart, liver, brain, and
Subhakti, M., Pramaningtyas, M., Prabowo, R. and Lusiantari, R.
The Effects of Administering Jicama Concentrate (Pachyrhizus erosus) and Kefir Grains as a Synbiotic Drink on Malondialdehyde and Superoxide Dismutase Levels in the Testicles of
Hyperlipidemic Rats.
DOI: 10.5220/0010490502310236
In Proceedings of the 1st Jenderal Soedirman International Medical Conference in conjunction with the 5th Annual Scientific Meeting (Temilnas) Consortium of Biomedical Science Indonesia
(JIMC 2020), pages 231-236
ISBN: 978-989-758-499-2
Copyright
c
2021 by SCITEPRESS – Science and Technology Publications, Lda. All rights reserved
231
testes. An increasing cholesterol level in the testicular
tissue results in excessive production of free radicals
(ROS) and oxidative stress. In the end, such condition
will have cytotoxic effects on spermatozoa
(Permatasari & Widhiantara, 2017).
Oxidative stress in the testicular tissue can cause
abnormalities in sperm quality and quantity, thus
leading to sperm DNA fragmentation and
transformation. Abnormal genetic material causes
imperfect transmission of genetic information the
embryo. Meanwhile, oxidative stress leads to
increased DNA damage. Free radicals can also result
in lipid peroxidation in the sperm cell membrane, and
the damage of which will decrease the ability of the
sperm to bind to oocytes (Asadi et al., 2017). The
Increasing damage of DNA and cell membrane of
spermatozoa results in infertility in men. The lipid
peroxidation of cell membrane will form
Malondialdehyde (MDA) molecules. The high
production of MDA will induce cell death in the
presence of a biomolecular damage process in these
cells (Ayala et al., 2014). The most effective
biomarker for assessing cell damage due to lipid
oxidative stress is MDA. It is necessary to note that
to date the damage caused by lipid peroxidation
becomes the most important factor of testicular
dysfunctions (Asadi et al., 2017).
Therapy to overcome hyperlipidemia continues to
evolve. The use of pharmacology from the statin class
remains a popular choice for patients with
hyperlipidemia since the side effects of statins on the
urology system rarely occur. However, such rare
occurrence should not be ignored by the doctor or
other healthcare providers. Linnebur and Hiatt in their
case report showed that a man (54 years) with
hyperlipidemia who received statins complained of
discomfort due to the pain in the testicles after a few
months of taking the drug (Linnebur & Hiatt, 2007).
Experts develop a new concept of disease
treatment with food as medicine. The concept is
rated to become a means to optimize food function as
a therapy against a disease. Kefir is made from cow,
goat, or sheep milk, which is fermented by a type of
starter called kefir grains (Wahdania & Pramono,
2012). Kefir made from cow milk and/or goat milk
can inhibit lipid peroxidation more significantly than
ordinary dairy of cows and/or goats (Liu et al., 2005).
Jicama or Pachyrhizus erosus which comes from
America and then grows widely in Indonesia is
among the root crops with consumable tubers. It is a
species of yam containing water, flour, vitamin C, B1,
and minerals such as calcium, phosphate, and
potassium (Widiyanti et al., 2018). Jicama can serve
as a prebiotic source with fructooligosaccharide
(FOS) and inulin content. Prebiotics are defined as
indigestible food components with such properties as
being resistant to stomach acid and hydrolysis by the
enzymes in the digestive system, being fermentable
by the gastrointestinal microflora, and having a
selective positive effect to stimulate bacterial growth
in the gastrointestinal tract (Bruggencate et al., 2006).
Synbiotics are a product which contains a
combination of probiotics and prebiotics (Abed et al.,
2016). This combination is useful to protect
probiotics when going through various processes in
the digestive tract16, thereby increasing the number
of intestinal microflora and optimizing its activity in
the body (Markowiak & Ślizewska, 2017). Based on
the aforementioned background, this study aims to
examine the effects of the administration of jicama
extract (Pachyrhizus erosus) and kefir grains as a
synbiotic drink on the levels of malondialdehyde
(MDA) and superoxide dismutase (SOD) activity in
the testes of rats with induced hyperlipidemia.
2 MATERIAL AND METHODS
This was a quasi-experimental study with a post-test
only controlled group design. The subjects were male
Wistar rats (Rattus norvegicus) aged 2-3 months with
a bodyweight ranging from 100-300 grams. The
number of rats used as the subjects followed the
criteria from the World Health Organization (WHO),
namely a minimum of five (5) rats in each treatment
group or using the Federer's formula.
The combination of jicama and kefir grain
synbiotic drink was prepared through several
processes. First, to prepare the kefir milk, kefir grains
were mixed with pasteurized fresh milk in a bottle at
the ratio of 1:20 (100 g kefir:2 liters of milk) and
fermented for 12 hours at a room temperature (25
0
C
– 27
0
C) in a dark state.
After 12 hours, the kefir grains were strained to
obtain the filtrate as kefir milk resulted from
fermentation. The kefir milk was then added to
pasteurized jicama juice (at a temperature of 80
0
C -
90
0
C) at the following ratio for each formulation. The
kefir milk and jicama juice from each formulation
was then mixed and re-fermented for 12 hours at
room temperature (25
0
C - 27
0
C) in the dark. After 12
hours, the fermentation product was stored in a
refrigerator at a temperature of 4°C (Mirdalisa et al.,
2016).
A total of 25 rats were divided evenly into 5
groups, including the positive control group (K+),
negative control group (K-), and 3 treatment groups
of P1 (85% milk, 15% jicama), P2 (75% milk, 25%
JIMC 2020 - 1’s t Jenderal Soedirman International Medical Conference (JIMC) in conjunction with the Annual Scientific Meeting
(Temilnas) Consortium of Biomedical Science Indonesia (KIBI )
232
jicama), and P3 (65% milk, 35% jicama). The K+
group and treatment groups were induced by quail
egg yolk at a dose of 5ml/200grBW given once a day
for 4 weeks through a feeding tube (Prabowo &
Pramaningtyas, 2018). The blood samples were
collected via the eye vein (Plexus retroorbital) for 3-
5 ml after each rat was anesthetized with 0.1-0.3 cc
ketamine-xylazine injected intraperitoneally.
The synbiotic drink was administered at a dose of
5ml/200grBW to the treatment groups once a day for
4 weeks through a feeding tube (Sudiarto et al., 2018).
The rats were then given 0.1-0.3 ml ketamine-
xylazine anesthetic intraperitoneally and decapitated.
Surgery was performed to remove the testicular
organs, which were then cleaned in NaCl solution,
wrapped in aluminum foil, and stored in a refrigerator
at -4°C.
The measurement of MDA levels used the
reaction principle of 0.67% TBA and 20% TCA while
SOD activity was measured using the Ransod kit. All
of the measurements were carried out at UGM Inter-
University Center. The bivariate data analysis was
employed to determine the effects of synbiotic drink
administration on MDA levels and SOD activity in
the testicular tissue.
Table 1. Formulations of synbiotic drink
Formulation Kefir (ml) Jicama Total
P1
85%
(255 ml)
15%
(45 ml)
300 ml
P2
75%
(225 ml)
25%
(75 ml)
300 ml
P3
65%
(195 ml)
35%
(105 ml)
300 ml
Total 675 ml 225 ml
3 RESULTS
The administration of high-fat diet for 4 weeks has
induced hyperlipidemia in the rats. After the egg yolk
administration was complete, the rats in K+ group
were given only ad libitum food, while the
intervention groups were given a synbiotic drink.
Four weeks later, the rats were terminated and the
levels of MDA and SOD were checked. In K+ and K-
groups, there were significant differences in the levels
of MDA and SOD. In the second 4 weeks, the
hyperlipidemic state is likely to be maintained by the
endogenous mechanisms of lipid metabolism.
Table 2. Average levels of Malondialdehyde (MDA)
Superoxide dismutase (SOD)
Group MDA
(nmol/gr)
p SOD
(%)
p
K+
K-
P1
P2
P3
12.30 ± 0.28
2.83 ± 0.27
8.43 ± 0.38
6.34 ± 0.29
4.49 ± 0.25
0,000 32.86 ± 6.75
82.14 ± 7.57
43.21 ± 5.56
62.14 ± 7.40
70.35 ± 4.82
0,000
Based on the bonferoni post-hoc test, it was found
that the P3 synbiotic drink formulation gave the best
effects as opposed to the P1 and P2 synbiotic drink
formulations. The P3 formulation is composed of
35% prebiotics and 65% probiotics. Giving synbiotic
drinks can reduce MDA levels in the testicular tissue.
This is proved by the One-way ANOVA test with p
<0.05.
4 DISCUSSIONS
Quail egg yolk in this research can induce
hyperlipidemia. Research conducted by Kusuma
proved that induction by quail egg yolk at a dose of
10 ml/KgBW for 14 days increased cholesterol levels.
Quail egg yolks contain numerous saturated fatty
acids which, through the beta-oxidation reaction, are
converted into acetyl CoA as a precursor for
cholesterol synthesis. The more acetyl CoA is
formed, the more it triggers the endogenous pathway
for cholesterol synthesis (Kusuma et al., 2016).
This is in line with the research by Prabowo and
Pramaningtyas in which a high-fat diet in the form of
quail egg yolk administered for 4 weeks can induce
hyperlipidemia in rats (Prabowo & Pramaningtyas,
2018). Hyperlipidemia in rats is characterized by total
cholesterol levels >130 mg/dl, LDL >60 mg/dl,
triglycerides >100 mg/dl, and HDL <50 mg/dl
(Cahyaji, 2017).
Triglycerides and cholesterol will form micellar
clots with other substances mediated by bile salts.
Triglycerides are hydrolyzed into fatty acids and then
absorbed by the intestine via the enterocyte cells. In
the enterocyte cell, a lipoprotein in the form of a
chylomicron will be produced which is composed of
fatty acids, cholesterol esters, and apo B-48 as the
main structural apolipoprotein in chylomicrons.
The Effects of Administering Jicama Concentrate (Pachyrhizus erosus) and Kefir Grains as a Synbiotic Drink on Malondialdehyde and
Superoxide Dismutase Levels in the Testicles of Hyperlipidemic Rats
233
Chylomicrons are formed in the lymph tissue and
then pass through the thoracic duct and enter the
blood circulation. Most of the cholesterols in
chylomicrons will be stored in the liver. High levels
of cholesterols in the hepatic tissue inhibit cholesterol
synthesis and degrade LDL receptors bound by
PCSK9 (Mehta & Bhatt, 2017).
Cholesterols in the liver tissue are released into
the blood circulation through VLDL, IDL, and LDL
lipoproteins. After the exogenous pathway stops,
cholesterols in the hepatic tissue will decrease, thus
triggering cholesterol synthesis by the hepatocyte
cells. Also, the high cholesterol precursor in the form
of acetyl CoA will further trigger the synthesis of
cholesterols (Kusuma et al., 2016). Therefore, the
oxidative stress and lipid peroxidation in tissues,
especially of the testes, remain high with increasing
levels of MDA.
The provision of synbiotic drink, a combination of
kefir grains and jicama juice, can reduce MDA levels
and increase SOD activity (Zhao et al., 2020). Kefir
grains contain a number of species of probiotic
bacteria, including lactic acid bacteria and acetic acid
bacteria. Besides, kefir grains contain yeast and fungi
(Pogačić et al., 2013).
In this research, P3 group give the best result in
decrease of MDA and increase SOD. This is
supported by the research conducted by Al-Sultan
which explained that the provision of synbiotic drinks
is better than only prebiotics or probiotics to improve
the function of the gut microflora in chickens. A
combination of synbiotics can help optimize the
management of hyperlipidemic conditions. Prebiotics
protect probiotics from various enzyme activities in
the digestive system. Therefore, the number of
probiotics reaching the intestine will increase,
resulting in optimal function of the intestinal
microflora (Al-Sultan et al., 2016). A combination of
synbiotics can help optimize the management of
hyperlipidemic conditions. Prebiotics protect
probiotics from various enzyme activities in the
digestive system. Therefore, the number of probiotics
reaching the intestine will increase, resulting in
optimal function of the intestinal microflora (Alves et
al., 2016).
Prebiotics contain inulin and FOS, which are
carbohydrates that cannot be digested by the human
intestine. Inulin and FOS have anti-hyperlipidemic
effects, but must first be fermented into short-chain
fatty acids (SCFA), namely acetate, propionate, and
butyrate. The fermentation of inulin and FOS into
SCFA can be mediated by the activity of the intestinal
microflora. Therefore, the more optimal the intestinal
microflora is, the more easily the inulin and FOS will
be fermented. The result of fermentation in the form
of SCFA can act as a HMGCoA-reductase inhibitor
to manage endogenous hyperlipidemia conditions
(Alves et al., 2016; Daliri et al., 2016).
The high LDL that accumulates in the testicular
tissue increases the production of free radicals (ROS)
since LDL is easily oxidized. A ROS chain reaction
will induce DNA damage and PUFA peroxidation in
testicular tissue cells. Probiotics can help overcome
this damage by managing hyperlipidemia, thereby
reducing the damage to the testicular tissue due to free
radicals. Also, probiotics increase the action of
antioxidants such as SOD, GPx, and catalase. These
enzymes can help to resolve oxidative stress states by
breaking the ROS chain and turning it into
nonreactive materials. A decrease in the state of
oxidative stress in the testicular tissue will inhibit the
abnormal condition of the cells in the tissue. The
quality of the spermatozoa produced will increase,
thus heightening the expectation to help overcome
male infertility and reduce the prevalence in the world
population of infertility (Amdekar & Singh, 2016;
Liu et al., 2005).
5 CONCLUSIONS
The administration of jicama juice (Pachyrhizus
erosus) and kefir grains as a synbiotic drink can
decrease malondialdehyde levels and increase
testicular superoxide dismutase activity in rats with
hyperlipidemia.
ACKNOWLEDGEMENTS
The authors would like to thank Miss Heni Ari Nur
Rohmawati for helping to proofread this manuscript
and Amiroh Dewi Kartika for helping prepare this
manuscript.
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