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In vivo effects of Viscum album and probiotics against carbon tetrachloride-induced liver injury

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Abstract

This study tested the possible protective and therapeutic effects of Viscum album extract and probiotics against carbon tetrachloride (CCl4)-induced acute/chronic liver injury. Male Wistar rats were assigned to seven groups: Control, acute CCl4, acute V. album + CCl4, acute V. album + Probiotics + CCl4, chronic CCl4, chronic CCl4 + V. album, and chronic CCl4 + V. album + Probiotics. Acute and chronic liver injuries were induced by 2 mg/kg CCl4 (i.p.) and 1 mg/kg CCl4 (i.p.), respectively. The extract and probiotics were administered daily to related groups. Serum enzyme activities, lipid profile, total protein, albumin, bilirubin, heme oxgenase-1 and 8-hydroxydeoxyguanosine levels were measured. Liver tissue sections stained with Hematoxylin-Eosin. Acute or chronic CCl4-exposure caused to significant changes in concentrations/activities of the measured parameters. The oral administration of extract and probiotics showed protective and therapeutic effects against CCl4-induced liver-injury. The supplementation of intestinal flora by the use of probiotics may enhance the efficacy of orally given therapeutic extracts.

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References

  • Abdel-Salam MO et al (2010) Effect of Viscum album on acute hepatic damage caused by carbon tetrachloride in rats. TurkJ Med Sci 40(3):421–426

    Google Scholar 

  • Adaramoye O, Amanlou M, Habibi-Rezaei M, Pasalar P, Ali MM (2012) Methanolic extract of African mistletoe (Viscum album) improves carbohydrate metabolism and hyperlipidemia in streptozotocin-induced diabetic rats. Asian Pac J Trop Med 5:427–433

    Article  CAS  Google Scholar 

  • Altamirano-Barrera A, Uribe M, Chávez-Tapia NC, Nuño-Lámbarri N (2018) The role of the gut microbiota in the pathology and prevention of liver disease. J Nutr Biochem 60:1–8

    Article  CAS  Google Scholar 

  • Bellassoued K, Hamed H, Ghrab F, Kallel R, Van Pelt J, Makni Ayadi F, Elfeki A (2019) Antioxidant and hepatopreventive effects of Cassia angustifolia extract against carbon tetrachloride-induced hepatotoxicity in rats. Arch Physiol Biochem:1–11. https://doi.org/10.1080/13813455.2019.1650778

  • Ben Hsouna A, Gargouri M, Dhifi W, Saibi W (2019) Antioxidant and hepato- preventive effect of Citrus aurantium extract against carbon tetrachloride-induced hepatotoxicity in rats and characterisation of its bioactive compounds by HPLC-MS. Arch Physiol Biochem 125:332–343

    Article  CAS  Google Scholar 

  • Beutler E (1986) Red cell metabolism. Churchill Livingstone, Edinburgh, New York

    Google Scholar 

  • Beutler E, Duron, O, Kelly BM (1963) Improved method for the determination of blood glutathione. J Lab Clin Med 61:882–888

  • Ćebović T, Spasić S, Popović M, Borota J, Leposavić G (2006) The European mistletoe (Viscum Album L.) grown on plums extract inhibits CCl4-induced liver damage in rats. Fresenius Environ Bull 15(5):393–400

    Google Scholar 

  • Celikkaya ME et al (2019) Effects of probiotic use on bacterial translocation in created rat models with biliary obstructions. Eurasian J Med 51:106–111

    Article  CAS  Google Scholar 

  • Cohen G, Dembiec D, Marcus J (1970) Measurement of catalase activity in tissue extracts. Anal Biochem 34:30–38

    Article  CAS  Google Scholar 

  • Dara L, Han D, Kaplowitz N (2013) Chapter 6 - mechanisms of cell death and relevance to drug toxicity. In: Kaplowitz N, DeLeve LD (eds) Drug-induced liver disease, 3rd edn. Academic Press, Boston, pp 101–122

  • Djurasevic S, Todorovic Z, Pavlovic S, Pejic S (2019) Chapter 27 - cadmium and fullerenes in liver diseases. In: Watson RR, Preedy VR (eds) Dietary interventions in liver disease. Academic Press, Boston, pp 333–344

  • Gharbi N, Pressac M, Hadchouel M, Szwarc H, Wilson SR, Moussa F (2005) [60]fullerene is a powerful antioxidant in vivo with no acute or subacute toxicity. Nano Lett 5:2578–2585

    Article  CAS  Google Scholar 

  • Gornall AG, Bardawill CJ, David MM (1949) Determination of serum proteins by means of the biuret reaction. J Biol Chem 177:751–766

    Article  CAS  Google Scholar 

  • Hegde P, Maddur MS, Friboulet A, Bayry J, Kaveri SV (2011) Viscum album exerts anti-inflammatory effect by selectively inhibiting cytokine-induced expression of cyclooxygenase-2. PLoS One 6:e26312

    Article  CAS  Google Scholar 

  • Khan RA, Khan MR, Sahreen S (2012) CCl4-induced hepatotoxicity: protective effect of rutin on p53, CYP2E1 and the antioxidative status in rat. BMC Complement Altern Med 12(1):178

  • Kuriakose J, Lal Raisa H, A. V, Eldhose B, M.S. L (2017) Terminalia bellirica (Gaertn.) Roxb. Fruit mitigates CCl4 induced oxidative stress and hepatotoxicity in rats. Biomed Pharmacother 93:327–333

    Article  CAS  Google Scholar 

  • Ljubuncic P, Tanne Z, Bomzon A (2000) Evidence of a systemic phenomenon for oxidative stress in cholestatic liver disease. Gut 47:710–716

    Article  CAS  Google Scholar 

  • Maheshwari DT, Yogendra Kumar MS, Verma SK, Singh VK, Singh SN (2011) Antioxidant and hepatoprotective activities of phenolic rich fraction of Seabuckthorn (Hippophae rhamnoides L.) leaves. Food Chem Toxicol 49:2422–2428

    Article  CAS  Google Scholar 

  • Manibusan MK et al (2007) Postulated carbon tetrachloride mode of action: a review. J Environ Sci Health C Environ Carcinog Ecotoxicol Rev 25:185–209

    Article  CAS  Google Scholar 

  • Nagy P, Thorgeirsson SS, Grisham JW (2020) Organizational principles of the liver. In: Arias IM, Alter HJ, Boyer JL, Cohen DE, Shafritz DA, Thorgeirsson SS, Wolkoff AW (eds) The liver. https://doi.org/10.1002/9781119436812.ch1

  • Nazaruk J, Orlikowski P (2016) Phytochemical profile and therapeutic potential of Viscum album L. Nat Prod Res 30:373–385

    Article  CAS  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  Google Scholar 

  • Onay-Ucar E et al (2006) Antioxidant activity of Viscum album ssp. album. Fitoterapia 77:556–560

    Article  Google Scholar 

  • Pritchard MT, Apte U (2015) Chapter 2 - models to study liver regeneration. In: Apte U (ed) Liver regeneration. Academic Press, Boston, pp 15–40

  • Rahmouni F, Saoudi M, Amri N, el-Feki A, Rebai T, Badraoui R (2018) Protective effect of Teucrium polium on carbon tetrachloride induced genotoxicity and oxidative stress in rats. Arch Physiol Biochem 124:1–9

    Article  CAS  Google Scholar 

  • Takahashi Y, Fukusato T (2017) Chapter 13 - animal models of liver diseases. In: Conn PM (ed) Animal models for the study of human disease, 2nd edn. Academic Press, Boston, pp 313–339

  • Thompson M et al (2017) Hepatotoxicity: treatment, causes and applications of medicinal plants as therapeutic agents. J Phytopharmacol 6(3):186–193

    Google Scholar 

  • Tröger W, Galun D, Reif M, Schumann A, Stanković N, Milićević M (2013) Viscum album [L.] extract therapy in patients with locally advanced or metastatic pancreatic cancer: a randomised clinical trial on overall survival. Eur J Cancer 49(18):3788–3797

  • Vidičević S et al (2019) Standardized Olea europaea L. leaf extract exhibits protective activity in carbon tetrachloride-induced acute liver injury in rats: the insight into potential mechanisms. Arch Physiol Biochem 126(5):1–9

  • Visschers RGJ, Luyer MD, Schaap FG, Olde Damink SWM, Soeters PB (2013) The gut-liver axis. Curr Opinion Clin Nutr Metab Care 16(5):576–581

  • Vulimiri SV, Pratt MM, Kulkarni S, Beedanagari S, Mahadevan B (2017) Chapter 21 - reproductive and developmental toxicity of solvents and gases. In: Gupta RC (ed) Reproductive and developmental toxicology, 2nd edn. Academic Press, Boston, pp 379–396

  • Wang MY, Anderson G, Nowicki D, Jensen J (2008) Hepatic protection by noni fruit juice against CCl(4)-induced chronic liver damage in female SD rats. Plant Foods Hum Nutr 63:141–145

    Article  CAS  Google Scholar 

  • Werthmann PG, Sträter G, Friesland H, Kienle GS (2013) Durable response of cutaneous squamous cell carcinoma following high-dose peri-lesional injections of Viscum album extracts--a case report. Phytomedicine 20:324–327

    Article  Google Scholar 

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Funding

This study supported by Scientific Research Projects Commission of the Eskisehir Osmangazi University (Project # 201711A137).

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Authors and Affiliations

  1. Department of Medical Biochemistry, Faculty of Medicine, Eskisehir Osmangazi University, Meselik Campus, 26480, Eskisehir, Turkey

    Meltem Erdaş, Fahrettin Akyüz, Betül Can & Mete Özkoç

  2. Department of Health Services, Vocational School of Health Services, Eskisehir Osmangazi University, Eskisehir, Turkey

    Semih Öz

  3. Department of Histology and Embryology, Faculty of Medicine, Eskisehir Osmangazi University, Eskisehir, Turkey

    Dilek Burukoğlu Dönmez

Authors
  1. Meltem Erdaş
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  2. Fahrettin Akyüz
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  3. Betül Can
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  4. Mete Özkoç
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  5. Semih Öz
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  6. Dilek Burukoğlu Dönmez
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Contributions

E. M. and A. F. designed the study. Ö. M. and Ö. S. performed surgical operations. E. M., C. B. and Ö. M. analyzed biochemical experiments. D. B. D. performed histological analyses. E. M. and C. B. wrote the paper and interpreted the data. All authors read and approved the final manuscript.

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Correspondence to Meltem Erdaş.

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Ethics approval

All animal research protocols in this study approved by the Institutional Ethics Committee (HADYEK, Protocol # 620/2017).

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The authors declare that they have no competing interests.

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Erdaş, M., Akyüz, F., Can, B. et al. In vivo effects of Viscum album and probiotics against carbon tetrachloride-induced liver injury. J Bioenerg Biomembr 53, 139–148 (2021). https://doi.org/10.1007/s10863-021-09883-7

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  • DOI: https://doi.org/10.1007/s10863-021-09883-7

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