Skip to main content

Advertisement

SpringerLink
Log in

Hypolipidemic and antioxidant effects of aqueous ethanolic extract from Moringa peregrina leaves on high-fat diet-induced fatty liver disease in rabbits

  • Original Article
  • Published:
Comparative Clinical Pathology Aims and scope Submit manuscript

Abstract

Moringa peregrina (M. peregrina) is a native species of Southwest Asia used to prepare traditional foods which have a wide range of antioxidants that can prevent metabolic disorders. The great interest has focused on the preparation and administration of herbal products to treat hyperlipidemia with fewer or no side effects along with economic and easy availability compared to conventional drugs. This study aimed to assess the lipid-lowering and antioxidant effects of aqueous ethanolic extract of M. peregrina leaves on fatty liver disease (NAFLD) model in rabbits as well as morphological changes, cytotoxic, and anti-lipid peroxidation effects of M. peregrine leaf extract (MPLE) on human umbilical vein endothelial cells (HUVECs) in vitro. Thirty-two adult male rabbits received a standard diet or a high-fat diet (HFD) for 112 days. During days 56–112, the standard diet group received normal saline, and the HFD groups received normal saline, M. peregrina extract (200 mg/kg body weight) orally by gavage, or simvastatin (0.6 mg/kg body weight) orally by gavage. Lipid profile, glutathione content, antioxidant enzymes, lipid peroxidation, blood urea nitrogen (BUN), creatinine, alanine aminotransferase (ALT) and aspartate aminotransferase (AST), and liver histology were assessed. The morphological changes, cytotoxic, and anti-lipid peroxidation effects of MPLE were evaluated on HUVECs. Administration of MPLE and simvastatin alone improved the high-fat diet-induced dyslipidemia and lipid peroxidation in HFD rabbits. The results also showed that MPLE and simvastatin significantly decreased body weight, tissue and cellular malondialdehyde (MDA) content, and serum tumor necrosis factor-alpha (TNF-α) (P < 0.001), and improved the antioxidant enzyme of rabbits fed HFD. Besides, MPLE induced time- and concentration-dependent in vitro cytotoxicity on HUVECs. Histopathological appearance of liver tissue confirmed the beneficial effect of the extract. Our results showed that MPLE might be a candidate agent for preventing NAFLD due to its lipid-lowering and antioxidative potentials.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5 
Fig. 6
Fig. 7
Fig. 8
Fig. 9

Similar content being viewed by others

Data availability

The data that support the findings of this study are available from the corresponding author upon reasonable request.

References

  • Abdel-Maksoud HA, Hussein MA, Afaf D, Abd El Mageed AD, Taha WA (2015) Biochemical effect of Moringa peregrina seeds on experimentally leukcytopenia in rats. Benha Vet Med J 29(1):151–163

    Article  Google Scholar 

  • Al-Aboudi A, Afifi FU (2011) Plants used for the treatment of diabetes in Jordan: a review of scientific evidence. Pharm Biol 49(3):221–239

    Article  PubMed  Google Scholar 

  • Alkhudhayri DA, Osman MA, Alshammari GM, Al Maiman SA, Yahya MA (2021) Moringa peregrina leaf extracts produce anti-obesity, hypoglycemic, anti-hyperlipidemic, and hepatoprotective effects on high-fat diet fed rats. Saudi J Biol Sci 28(6):3333–3342

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Al-Owaisi M, Al-Hadiwi N, Khan SA (2014) GC-MS analysis, determination of total phenolics, flavonoid content and free radical scavenging activities of various crude extracts of Moringa peregrina (Forssk.) Fiori leaves. Asian Pac J Trop Biomed 4(12):964–970

  • Al-Quran S (2008) Taxonomical and pharmacological survey of therapeutic plants in Jordan. J Nat Prod 1:10–26

    Google Scholar 

  • Azim SA, Abdelrahem MT, Said MM, Khattab A (2017) Protective effect of Moringa peregrina leaves extract on acetaminophen-induced liver toxicity in albino rats. Afr J Tradit Complement Altern Med 14(2):206–216

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen X, Li X, Xu X, Li LN, Zhang L, Lv J, Wu YC, Yin H (2021) Ferroptosis and cardiovascular disease: role of free radical-induced lipid peroxidation. Free Radical Res 55(4):405–415

    Article  CAS  Google Scholar 

  • Djeridane A, Yousfi M, Nadjemi B, Boutassouna D, Stocker P, Vidal N (2006) Antioxidant activity of some Algerian medicinal plants extracts containing phenolic compounds. Food Chem 97(4):654–660

    Article  CAS  Google Scholar 

  • El Baky HA, El-Baroty GS (2013) Characterization of Egyptian Moringa peregrina seed oil and its bioactivities. Int J Manag Sci Bus Res 2:98–108

    Google Scholar 

  • El-Alfy TS, Ezzat SM, Hegazy AK, Amer AM, Kamel GM (2011) Isolation of biologically active constituents from Moringa peregrina (Forssk.) Fiori. (family: Moringaceae) growing in Egypt. Pharm Mag 7(26):109

  • Elarabany N, Hamad A, AlSobeai SM (2022) Evaluating anti-obesity potential, active components, and antioxidant mechanisms of Moringa peregrina seeds extract on high-fat diet-induced obesity. J Food Biochem 46(10):e14265

    Article  CAS  PubMed  Google Scholar 

  • El-Awady MA, Hassan MM, Abdel-Hameed ES, Gaber A (2015) Comparison of the antimicrobial activities of the leaves-crude extracts of Moringa peregrina and Moringa oleifera in Saudi Arabia. Int J Curr Microbiol Appl Sci 4(12):1–9

    CAS  Google Scholar 

  • Ellman GL (1959) Tissue sulfhydryl groups. Arch Biochem Biophys 82(1):70–77

    Article  CAS  PubMed  Google Scholar 

  • Elsayed EA, Sharaf-Eldin MA, El-Enshasy HA, Wadaan M (2016) In vitro assessment of anticancer properties of Moringa peregrina essential seed oil on different cell lines. Pakistan J Zool 48(3):853–859

    CAS  Google Scholar 

  • Gazzola K, Vigna GB (2016) Hypolipidemic drugs in elderly subjects: indications and limits. Nutr Metab Cardiovasc Dis 26(12):1064–1070

    Article  CAS  PubMed  Google Scholar 

  • Ghazanfar SA, Al-Al-Sabahi AM (1993) Medicinal plants of northern and central Oman (Arabia). Econ Bot 47(1):89–98

    Article  Google Scholar 

  • Goth L (1991) A simple method for determination of serum catalase activity and revision of reference range. Clin Chim Acta 196:143–151

    Article  CAS  PubMed  Google Scholar 

  • Hasani-Ranjbar S, Nayebi N, Moradi L, Mehri A, Larijani B, Abdollahi M (2010) The efficacy and safety of herbal medicines used in the treatment of hyperlipidemia; a systematic review. Curr Pharm Des 16(26):2935–2947

    Article  CAS  PubMed  Google Scholar 

  • Hegazy AK, Hammouda O, Lovett-Doust J, Gomaa NH (2008) Population dynamics of Moringa peregrina along altitudinal gradient in the northwestern sector of the Red Sea. J Arid Environ 72(9):1537–1551

    Article  Google Scholar 

  • Hodek P, Trefil P, Stiborová M (2002) Flavonoids-potent and versatile biologically active compounds interacting with cytochromes P450. Chem Biol Interact 139(1):1–21

    Article  CAS  PubMed  Google Scholar 

  • Jollow DJ, Mitchell JR, Zampaglione N, Gillette JR (1974) Bromobenzene induced liver necrosis. Protective role of glutathione and evidence for 3,4-bromobenzene oxide as the hepatotoxic metabolites. Pharmacology 11(3):151–169

  • Juhaimi FA, Ghafoor K, Ahmed IM, Babiker EE, Özcan MM (2017) Comparative study of mineral and oxidative status of Sonchus oleraceus, Moringa oleifera and Moringa peregrina leaves. J Food Meas Charact 11:1745–1751

    Article  Google Scholar 

  • Kruger NJ, Walker JM (2009) The Bradford method for protein quantitation. In The protein protocols handbook (pp. 17–24). Humana Press, Totowa, NJ

  • Lalas S, Gortzi O, Athanasiadis V, Tsaknis J, Chinou I (2012) Determination of antimicrobial activity and resistance to oxidation of Moringa peregrina seed oil. Molecules 17(3):2330–2334

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lamarche B, Després JP, Moorjani S, Cantin B, Dagenais GR, Lupien PJ (1996) Triglycerides and HDL-cholesterol as risk factors for ischemic heart disease. Results from the Quebec cardiovascular study. Atherosclerosis 119(2):235–245

  • Lee IS, Shin G, Choue R (2009) Shifts in diet from high fat to high carbohydrate improved levels of adipokines and pro-inflammatory cytokines in mice fed a high-fat diet. Endocr J 57(1):39–50

    Article  PubMed  Google Scholar 

  • Luqman S, Srivastava S, Kumar R, Maurya AK, Chanda D (2012) Experimental assessment of Moringa oleifera leaf and fruit for its antistress, antioxidant, and scavenging potential using in vitro and in vivo assays. Evid Based Compl Alt Article ID 519084

  • Majali I, Althunibat O, Qaralleh H (2015) Antimicrobial and immunomodulatory activities of Moringa peregrina-MINIREVIEW. J Basic Appl Res Int 1(2):55–61

    Google Scholar 

  • Marwah RG, Fatope MO, Al Mahrooqi R, Varma GB, Al Abadi H, Al-Burtamani SK (2007) Antioxidant capacity of some edible and wound healing plants in Oman. Food Chem 101(2):465–470

    Article  CAS  Google Scholar 

  • Morgan DM (1998) Tetrazolium (MTT) assay for cellular viability and activity. InPolyamine protocols (pp. 179–184). Humana Press

  • 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  PubMed  Google Scholar 

  • Osman HE, Abohassan AA (2012) Morphological and analytical characterization of Moringa peregrina population in Western Saudi Arabia. Int J Theor Appl Sci 4(2):174–184

  • Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxid Med Cell Longev 2(5):270–278

    Article  PubMed  PubMed Central  Google Scholar 

  • Pearson TA (1999) Cardiovascular disease in developing countries: myths, realities, and opportunities. Cardiovasc Drugs Ther 13(2):95–104

    Article  CAS  PubMed  Google Scholar 

  • Rouhi-Broujeni H, Heidarian E, Darvishzadeh-Boroojeni P, Rafieian-Kopaei M, Gharipour M (2013) Lipid lowering activity of Moringa peregrina seeds in rat: a comparison between the extract and atorvastatin. Res J Biol Sci 8(5):150–154

    Google Scholar 

  • Saravani R, Sargazi S, Saravani R, Rabbani M, Rahdar A, Taboada P (2020) Newly crocin-coated magnetite nanoparticles induce apoptosis and decrease VEGF expression in breast carcinoma cells. J Drug Deliver Sci Tech 60:101987

    Article  CAS  Google Scholar 

  • Sibouakaz D, Othmani-Mecif K, Fernane A, Taghlit A, Benazzoug Y (2018) Biochemical and ultrastructural cardiac changes induced by high-fat diet in female and male prepubertal rabbits. Anal Cell Pathol Article ID 6430696:1–16

    Google Scholar 

  • Sorokin A, Brown JL, Thompson PD (2007) Primary biliary cirrhosis, hyperlipidemia, and atherosclerotic risk: a systematic review. Atherosclerosis 194:293–299

    Article  CAS  PubMed  Google Scholar 

  • Speisky H, Cassels BK, Lissi EA, Videla LA (1991) Antioxidant properties of the alkaloid boldine in systems undergoing lipid peroxidation and enzyme inactivation. Biochem Pharmacol 41(11):1575–1581

    Article  CAS  PubMed  Google Scholar 

  • Stewart LK, Soileau JL, Ribnicky D, Wang ZQ, Raskin I, Poulev A, Majewski M, Cefalu WT, Gettys TW (2008) Quercetin transiently increases energy expenditure but persistently decreases circulating markers of inflammation in C57BL/6J mice fed a high-fat diet. Metabolism 57(7):39–46

    Article  Google Scholar 

  • Sun YI, Oberley LW, Li Y (1988) A simple method for clinical assay of superoxide dismutase. Clin Chem 34(3):497–500

    Article  CAS  PubMed  Google Scholar 

  • Theuwissen E, Mensink RP (2008) Water-soluble dietary fibers and cardiovascular disease. Physiol Behav 94(2):285–292

    Article  CAS  PubMed  Google Scholar 

  • Ullah MF, Bhat SH, Abuduhier FM (2015) Antidiabetic potential of hydro-alcoholic extract of Moringa peregrina leaves: implication as functional food for prophylactic intervention in prediabetic stage. J Food Biochem 39:360–367

    Article  CAS  Google Scholar 

Download references

Acknowledgements

We would like to express our sincere gratitude to M. Salehi Moghadam for his assistance in performing the research.

Author information

Authors and Affiliations

  1. Department of Basic Veterinary Sciences, Faculty of Veterinary Medicine, University of Zabol, Zabol, Iran

    Mohammad Reza Hajinezhad

  2. Special Domestic Animals Institute, Research Institute of Zabol, Zabol, Iran

    Amir Mokhtarpour

  3. Department of Animal Science, Gorgan University of Agricultural Sciences and Natural Resources, Gorgan, Iran

    Aazam Mirheidari

Authors
  1. Mohammad Reza Hajinezhad
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Amir Mokhtarpour
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Aazam Mirheidari
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Mohammad Reza Hajinezhad or Amir Mokhtarpour.

Ethics declarations

Funding

This work was supported by the University of Zabol (Grant number: UOZ.GR. 1821).

Conflict of interest

The authors declare that there is no conflict of interest.

Ethical approval

Experiments were performed in accordance with the Guide for the Care and Use of Laboratory Animals (from NIH Publication No. 85–23). The study protocol was also approved by the ethical committee at the University of Zabol, Zabol, Iran (IR.UOZ.REC.1398).

Informed consent

For this type of study, informed consent is not required.

Consent for publication

For this type of study, consent for publication is not required.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Hajinezhad, M.R., Mokhtarpour, A. & Mirheidari, A. Hypolipidemic and antioxidant effects of aqueous ethanolic extract from Moringa peregrina leaves on high-fat diet-induced fatty liver disease in rabbits. Comp Clin Pathol 32, 617–628 (2023). https://doi.org/10.1007/s00580-023-03470-5

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00580-023-03470-5

Keywords

Search

Navigation