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

, Miranti Dewi Pramaningtyas

, Rafik Prabowo

and Rokhima Lusiantari

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

https://orcid.org/0000-0003-4248-8393

https://orcid.org/0000-0003-1215-881X

https://orcid.org/0000-0003-0827-3591

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

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

– 27

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

C -

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

C - 27

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

85%

(255 ml)

15%

(45 ml)

300 ml

75%

(225 ml)

25%

(75 ml)

300 ml

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

(%)

K+

K-

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.

REFERENCES

Abed, S. M., Ali, A. H., & Noman, A. (2016). Inulin as

Prebiotics and its Applications in Food Industry and

Human Health ; A Review. International Journal of

Agriculture Innovations and Research, 5(1), 88–97.

Al-Sultan, S. I., Abdel-Raheem, S. M., El-Ghareeb, W. R.,

& Mohamed, M. H. A. (2016). Comparative effects of

using prebiotic , probiotic , synbiotic and acidifier on

growth performance , intestinal microbiology and

histomorphology of broiler chicks. Japanese Journal of

Veterinary Research, 64(Supplement 2), 187–195.

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 )

234

Alves, J. L. D. B., Sousa, V. P. De, Neto, M. P. C., Magnani,

M., Braga, V. D. A., & Costa-silva, J. H. (2016). New

Insights on the Use of Dietary Polyphenols or

Probiotics for the Management of Arterial

Hypertension. Frontiers in Psychology, 7(448), 1–8.

https://doi.org/10.3389/fphys.2016.00448

Amdekar, S., & Singh, V. (2016). Lactobacillus acidophilus

maintained oxidative stress from reproductive organs in

collagen-induced arthritic rats. Journal of Human

Reproductive Sciences, 9(1), 41–46.

https://doi.org/https://doi.org/10.4103/0974-

1208.178638

Asadi, N., Bahmani, M., Kheradmand, A., & Rafieian-

kopaei, M. (2017). The Impact of Oxidative Stress on

Testicular Function and the Role of Antioxidants in

Improving it : A Review. Journal of Clinical and

Diagnostic Research, 11(5), 1–5.

https://doi.org/10.7860/JCDR/2017/23927.9886

Ayala, A., Muñoz, M. F., & Argüelles, S. (2014). Lipid

Peroxidation : Production , Metabolism , and Signaling

Mechanisms of Malondialdehyde and 4-Hydroxy-2-

Nonenal. Oxidative Medicine and Cellular Longevity,

2014, 1–31.

https://doi.org/https://doi.org/10.1155/2014/360438

Bruggencate, S. J. M. Ten, Bovee-oudenhoven, I. M. J.,

Lettink-wissink, M. L. G., Katan, M. B., & Meer, R.

Van Der. (2006). Dietary Fructooligosaccharides

Affect Intestinal Barrier Function in Healthy Men. The

Journal of Nutrition, 136(1), 70–74.

https://doi.org/https://doi.org/10.1093/jn/136.1.70

Cahyaji, A. A. (2017). Pengaruh Aroma Terapi Minyak

Atsiri Jahe terhadap Kadar Trigliserida dan Kolesterol

Darah Tikus yang diberi Pakan tinggi Lemak [The

Effect of Aroma Therapy of Ginger Essential Oil on

Triglyceride Levels and Blood Cholesterol in Rats

given High Fat Feed]. Jurnal Wahana Peternakan,

1(2), 5–10.

Daliri, E. B., Lee, B. H., & Oh, D. H. (2016). Current

Perspectives on Antihypertensive Probiotics.

Probiotics and Antimicrobial Proteins, 9(2), 91–101.

https://doi.org/10.1007/s12602-016-9241-y

Inhorn, M. C., & Patrizio, P. (2015). Infertility around the

globe : new thinking on gender , reproductive

technologies and global movements in the 21st century.

Human Reproduction Update, 21(4), 411–426.

https://doi.org/10.1093/humupd/dmv016

Kusuma, A. M., Asarina, Y., Rahmawati, Y. I., & Susanti.

(2016). Efek Ekstrak Bawang Dayak ( Eleutherine

palmifolia ( L .) Merr ) dan Ubi Ungu ( Ipomoea batatas

L ) terhadap Penurunan Kadar Kolesterol dan

Trigliserida Darah pada Tikus Jantan [Effect of Dayak

Garlic (Eleutherine palmifolia (L.)Merr) Extract and

Sweet Pu. Junal Kefarmasian Indonesia, 6(2), 108–

116.

Linnebur, S. A., & Hiatt, W. H. (2007). Probable statin-

induced testicular pain. Annals of Pharmacotherapy,

41(1), 138–142. https://doi.org/10.1345/aph.1H444

Liu, J., Lin, Y., Chen, M., Chen, L., Lin, C., & Al, L. I. U.

E. T. (2005). Antioxidative Activities of Kefir. Asian-

Australasian Journal of Animal Sciences, 18(4), 567–

573.

https://doi.org/https://doi.org/10.5713/ajas.2005.567

Markowiak, P., & Ślizewska, K. (2017). Effects of

probiotics, prebiotics, and synbiotics on human health.

Nutrients, 9(9). https://doi.org/10.3390/nu9091021

Mehta, V., & Bhatt, K. (2017). Lipids and its Metabolism.

Journal of Cardiology & Cardiovascular Therapy,

4(2), 001–006.

https://doi.org/10.19080/JOCCT.2017.04.555635

Mirdalisa, C. A., Zakaria, Y., & Nurliana. (2016). Efek

Suhu dan Masa Simpan Terhadap Aktivitas

Antimikroba Susu Fermentasi dengan Lactobacillus

casei [Effects of temperature and storage time on the

antimicrobial activity fermented milk with

Lactobacillus casei]. Agripet, 16(1), 49–55.

https://doi.org/http://dx.doi.org/10.17969/agripet.v16i1

.3639

Nirosha, K., Divya, M., Vamsi, S., & Sadiq, M. (2014). A

review on hyperlipidemia. International Journal Of

Novel Trends In Pharmaceutical Sciences, 4(5), 81–92.

Permatasari, A. A. A. P., & Widhiantara, I. G. (2017).

Terapi Testosteron Meningkatkan Jumlah Sel Leydig

dan Spermatogenesis Mencit ( Mus Musculus ) yang

Mengalami Hiperlipidemia [Testosterone Therapy

Increases the Number of Leydig Cells and

Spermatogenesis in Mice (Mus Musculus) with

Hyperlipidemia]. Junal Media Sains, 1(22), 77–83.

Pogačić, T., Šinko, S., Zamberlin, Š., & Samaržija, D.

(2013). Microbiota of kefir grains. Mljekarstvo, 63(1),

3–14.

Prabowo, R., & Pramaningtyas, M. D. (2018). The Effect

of Combination Juice of Cucumber, Star Fruit and

Sweet Orange on The Lipid Profile of Hyperlipidemic

Rats (Rattus norvegicus). Clinical Hypertension. Jeju:

Korean Society of Hypertension, 294.

Pushpendra, A., & Jain, G. C. (2015). Hyper-Lipidemia and

Male Fertility: A Critical Review of Literature.

Andrology (Los Angel), 4(2).

https://doi.org/10.4172/2167-0250.1000141

Schisterman, E. F., Mumford, S. L., Chen, Z., Browne, R.

W., Barr, D. B., Kim, S., & Louis, G. M. B. (2014).

Lipid Concentrations and Semen Quality: The LIFE

Study Enrique. Andrology, 2(3), 408–415.

https://doi.org/10.1111/j.2047-

2927.2014.00198.x.Lipid

Sudiarto, Prabowo, R., & Pramaningtyas, M. D. (2018).

The Effect of Probiotic Beverage from Date Palm and

Kefir Grains on The Lipid Profile of Hyperlipidemic

Rats (Rattus norvegicus). In: International Congress of

Diabetes and Metabolism.

Wahdania, F., & Pramono, A. (2012). Pengaruh Pemberian

Kefir Susu Sapi Terhadap Kadar Kolesterol Total Tikus

Jantan Sprague Dawley [The Effect of Milk Kefir on

LDL Cholesterol Levels in Male Sprague dawley

Hypercholesterolemia Rats]. Journal of Nutrition

College,

1(1), 224–228.

https://doi.org/https://doi.org/10.14710/jnc.v1i1.386

Widiyanti, Y., Diana, W., Khairina, A., & Hasibuan, H.

(2018). Effect of Variation Time Storage of Jicama

(Pachyrrhizuserozus) to Cholesterol and Lypase

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

235

Activities Rattus norvegicus. International Conference

Postgraduate School (ICPSUAS 2017), 234–238.

Zhao, J., Yu, L., Zhai, Q., Tian, F., Zhang, H., & Chen, W.

(2020). Effects of probiotic administration on hepatic

antioxidative parameters depending on oxidative stress

models: A meta-analysis of animal experiments.

Journal of Functional Foods, 71(May), 103936.

https://doi.org/10.1016/j.jff.2020.103936

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 )

236