Skip to main content
Log in

Anti-helminthic effects and cellular mechanisms of Astragalus ecbatanus extract against Echinococcus granulosus protoscoleces

  • Original Article
  • Published:
Journal of Parasitic Diseases Aims and scope Submit manuscript

Abstract

We aimed to investigate the in vitro and ex vivo anti-helminthic effects of Astragalus ecbatanus chloroform extract (AECE) as well as its cellular mechanisms against Echinococcus granulosus protoscoleces. In vitro and ex vivo anti-helminthic effects of AECE on E. granulosus protoscoleces were evaluated through eosin exclusion test. Effects of AECE on induction of the caspase-3 like activity, the permeability of plasma membrane were also determined. The effects of AECE against the human hepatocyte carcinoma (HepG2) and human embryonic kidney (HEK293T) cells were determined by MTT ([3-(4.5-dimethylthiazol-2-yl)-2.5-diphenyl tetrazolium bromide)]) test. The findings revealed that AECE especially at 45 mg/mL displayed potent in vitro and ex vivo anti-helminthic effects against E. granulosus protoscoleces (p < 0.001). After treatment of protoscoleces with AECE, the caspase-3 enzyme activity and the rate of permeability of plasma membrane was dose dependently (P < 0.001) increased. The 50% cytotoxic concentration (CC50) value of AECE for normal and cancer cells lines 4.62 mg/mL and 1.89 mg/mL, respectively. The findings of the current study revealed the favorable in vitro and ex vivo anti-helminthic effects of AECE against protoscoleces of E. granulosus. However, further surveys in animal model are required to elucidate different aspects of this extract before use in clinical phases.

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

Access this article

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

Similar content being viewed by others

References

  • Agudelo Higuita NI, Brunetti E, McCloskey C (2016) Cystic echinococcosis. J Clin Microbiol 54(3):518–23. https://doi.org/10.1128/JCM.02420-15 (Epub 2015 Dec 16)

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Albalawi AE, Khalaf AK, Alyousif MS, Alanazi AD, Baharvand P, Shakibaie M, Mahmoudvand H (2021) Fe3O4@ piroctone olamine magnetic nanoparticles: synthesize and therapeutic potential in cutaneous leishmaniasis. Biomed Pharmacother 1(139):111566

    Article  Google Scholar 

  • Albayrak S, Kaya O (2018) Antioxidant and antimicrobial activities of four Astragalus species growing wild in Turkey. Turkish J Biochem 43(4):425–434. https://doi.org/10.1515/tjb-2017-0241

    Article  CAS  Google Scholar 

  • Anadol D, Ozçelik U, Kiper N, Göçmen A (2001) Treatment of hydatid disease. Paediatr Drugs 3(2):123–135. https://doi.org/10.2165/00128072-200103020-00005

    Article  CAS  PubMed  Google Scholar 

  • Bratkov VM, Shkondrov AM, Zdraveva PK, Krasteva IN (2016) Flavonoids from the genus Astragalus: phytochemistry and biological activity. Pharmacogn Rev 10(19):11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheraghipour K, Beiranvand M, Zivdari M, Amiri S, Masoori L, Nourmohammadi M, Ali AS, Abbaszadeh S, Moradpour K, Marzban A (2021) In vitro potential effect of Pipper longum methanolic extract against protoscolices of hydatid cysts. Exp Parasitol 221:108051

    Article  CAS  PubMed  Google Scholar 

  • Cushnie TP, Lamb AJ (2005) Antimicrobial activity of flavonoids. Int J Antimicrob Agents 26(5):343–356

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ebadi AR, Monadi A, Pashazadeh M, Zakhireh S (2014) Antibacterial effects alcholic extracts of (Astragalus hamosus) on gram positive and gram negative bacteria. J Comp Pathobiol Iran 10:1071–1076

    Google Scholar 

  • Echert J, Thompson RC (2017) Historical aspects of echinococcosis. Adv Parasitol 95:1–64. https://doi.org/10.1016/bs.apar.2016.07.003 (Epub 2016 Sep 29)

    Article  Google Scholar 

  • Epand RM, Walker C, Epand RF, Magarvey NA (2016) Molecular mechanisms of membrane targeting antibiotics. Biochim et Biophys Acta (BBA) - Biomembranes 5:980–987

    Article  Google Scholar 

  • Evans WC (1998) Trease and Evans Pharmacognosy, 14th edn. WB Saunders, Philadelphia

    Google Scholar 

  • Ezzatkhah F, Khalaf AK, Mahmoudvand H (2021) Copper nanoparticles: biosynthesis, characterization, and protoscolicidal effects alone and combined with albendazole against hydatid cyst protoscoleces. Biomed Pharmacother 1(136):111257

    Article  Google Scholar 

  • Ghasemian-Yadegari J, Nazemiyeh H, Asnaashari S, Fathiazad F (2015) Chemical characterization of the essential oil from aerial parts of Astragalus maximus from Northwest of Iran. Adv Biosci Clin Med 3(3):32–39

    Google Scholar 

  • Giorgio A, Di Sarno A, de Stefano G, Farella N, Matteucci P, Scognamiglio U, Giorgio V (2009) Percutaneous treatment of hydatid liver cyst. Recent Pat Antiinfect Drug Discov 4(1):29–36. https://doi.org/10.2174/157489109787236274

    Article  CAS  PubMed  Google Scholar 

  • Górniak I, Bartoszewski R, Króliczewski J (2019) Comprehensive review of antimicrobial activities of plant flavonoids. Phytochem Rev 18(1):241–272

    Article  Google Scholar 

  • Guo L, Sun Y, Ping X, Liu J, Wang X, Qin N (2021) Chemical composition and antibacterial activity of ethyl acetate extract of Astragalus membranaceus aerial parts. J Food Safety. https://doi.org/10.1111/jfs.12947

    Article  Google Scholar 

  • i Gavara CG, López-Andújar R, Ibáñez TB, Ángel JM, Herraiz ÁM, Castellanos FO, Ibars EP, Rodríguez FS (2015) Review of the treatment of liver hydatid cysts. World J Gastroenterol WJG 21(1):124

    Article  Google Scholar 

  • Jun YM, Kim EH, Lim JJ, Kim SH, Kim SH, Lim JD, Cheoi DS, Cheoi YS, Yu CY, Chung IM (2012) Variation of phenolic compounds contents in cultivated Astragalus membranaceus. Korean J Med Crop Sci 20(6):447–453

    Article  Google Scholar 

  • Junghanss T, da Silva AM, Horton J et al (2008) Clinical management of cystic echinococcosis: state of the art, problems, and perspectives. Am J Trop Med Hyg 79(3):301–311

    Article  PubMed  Google Scholar 

  • Kern P, Menezes da Silva A, Akhan O, Müllhaupt B, Vizcaychipi KA, Budke C, Vuitton DA (2017) The Echinococcoses: diagnosis, clinical management and burden of disease. Adv Parasitol 96:259–369. https://doi.org/10.1016/bs.apar.2016.09.006 (Epub 2017 Feb 8)

    Article  CAS  PubMed  Google Scholar 

  • Kheirandish F, Marzban A, Masoori L, Nourmohammadi M, Moradpour K, Cheraghipour K (2020) Efficacy of thymol on the scolices of hydatid cyst. Herb Med J 28:37–44

    Google Scholar 

  • Li X, Qu L, Dong Y, Han L, Liu E, Fang S, Zhang Y, Wang T (2014) A review of recent research progress on the Astragalus genus. Molecules 19(11):18850–18880

    Article  PubMed  PubMed Central  Google Scholar 

  • Mahmoudvand H, Mahmoudvand H, Oliaee RT, Kareshk AT, Mirbadie SR, Aflatoonian MR (2017) In vitro protoscolicidal effects of Cinnamomum zeylanicum essential oil and its toxicity in mice. Pharmacogn Mag 13(Suppl 3):S652

    PubMed  PubMed Central  Google Scholar 

  • Mahmoudvand H, Saki M, Kiani AA, Taban T, Shahmoradi MK (2021) In vitro and ex vivo antiparasitic Effect of Rheum ribes L. extract against the hydatid cyst protoscoleces. Infect Dis-Drug Targets (Formerly Current Drug Targets-Infectious Disorders) 21(6):47–52

    Google Scholar 

  • Masoumi-Ardakani Y, Mahmoudvand H, Mirzaei A, Esmaeilpour K, Ghazvini H, Khalifeh S, Sepehri G (2017) The effect of Elettaria cardamomum extract on anxiety-like behavior in a rat model of post-traumatic stress disorder. Biomed Pharmacother 1(87):489–495

    Article  Google Scholar 

  • Mead J, McNair N (2006) Antiparasitic activity of flavonoids and isoflavones against Cryp-tosporidium parvum and Encephalitozoon intestinalis. FEMS Microbiol Lett 259(1):153–157

    Article  CAS  PubMed  Google Scholar 

  • Miraj S, Kiani S (2016) Astragalus membranaceus: a review study of its anti-carcinoma activities. Pharm Lett 8(6):59–65

    Google Scholar 

  • Niazi M, Saki M, Sepahvand M, Jahanbakhsh S, Khatami M, Beyranvand M (2019) In vitro and ex vivo scolicidal effects of Olea europaea L. to inactivate the protoscolecs during hydatid cyst surgery. Ann Med Surg 42:7–10

    Article  Google Scholar 

  • Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci. https://doi.org/10.1017/jns.2016.41

    Article  PubMed  PubMed Central  Google Scholar 

  • Phuyal N, Jha PK, Raturi PP, Rajbhandary S (2020) Total phenolic, flavonoid contents, and antioxidant activities of fruit, seed, and bark extracts of Zanthoxylum armatum DC. Sci World J 16:2020

    Google Scholar 

  • Portt L, Norman G, Clapp C, Greenwood M, Greenwood MT (2011) Anti-apoptosis and cell survival: a review. Biochim et Biophys Acta (BBA) - Mol Cell Res 1813:238–259

    Article  CAS  Google Scholar 

  • Rajabi MA (2009) Fatal reactions and methaemoglobinaemia after silver nitrate irrigation of hydatid cyst. Surg Pract 13:2–7

    Article  Google Scholar 

  • Ramírez-Macías I, Marín C, Díaz JG, Rosales MJ, Gutiérrez-Sánchez R, Sánchez-Moreno M (2012) Leishmanicidal activity of nine novel flavonoids from Delphinium staphisagria. Sci World J 2012:203646

    Article  Google Scholar 

  • Rasoulian B, Hajializadeh Z, Esmaeili-Mahani S, Rashidipour M, Fatemi I, Kaeidi A (2019) Neuroprotective and antinociceptive effects of rosemary (Rosmarinus officinalis L.) extract in rats with painful diabetic neuropathy. J Physiol Sci 69(1):57–64

    Article  CAS  PubMed  Google Scholar 

  • Rios JL, Waterman PG (1997) A review of the pharmacology and toxicology of Astragalus. Phytother Res Int J Dev Med Sci Res Plants Plant Prod 11(6):411–418

    CAS  Google Scholar 

  • Salimikia I, Hakami M, Shahmoradi MK (2021) Iranian herbal medicines against hydatid cyst protoscoleces: a systematic review. Infect Dis-Drug Targ 21(5):38–44

    Google Scholar 

  • Sedighi M, Nazari A, Faghihi M, Rafieian-Kopaei M, Karimi A, Moghimian M, Mozaffarpur SA, Rashidipour M, Namdari M, Cheraghi M, Rasoulian B (2018) Protective effects of cinnamon bark extract against ischemia–reperfusion injury and arrhythmias in rat. Phytother Res 32(10):1983–1991

    Article  CAS  PubMed  Google Scholar 

  • Shahrajabian MH, Sun W, Cheng Q (2019) A review of Astragalus species as foodstuffs, dietary supplements, a traditional Chinese medicine and a part of modern pharmaceutical science. Appl Ecol Environ Res 17(6):13371–13382

    Article  Google Scholar 

  • Shakib P, Sheikhian A, Moradpour K, Kalani H, Zebardastpour M, Cheraghipour K, Beiranvand M (2022) In vivo and In vitro anti-hydatidosis effect of garlic: a systematic review. Current Drug Therapy 17(1):12–16

    Article  Google Scholar 

  • Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) Analysis of total phenols and other oxidation substrates and antioxidants by means of folin-ciocalteu reagent. Methods Enzymol 299:152–178

    Article  CAS  Google Scholar 

  • Solomon N, Fields PJ, Tamarozzi F, Brunetti E, Macpherson CNL (2017) Expert reliability for the world health organization standardized ultrasound classification of cystic echinococcosis. Am J Trop Med Hyg. 96(3):686–691. https://doi.org/10.4269/ajtmh.16-0659

    Article  PubMed  PubMed Central  Google Scholar 

  • Turgut-Kara N, Arı S (2006) Micropropagation of Astragalus maximus willd. Biotechnol Biotechnol Equip 20(1):20–22

    Article  CAS  Google Scholar 

  • Wen H, Vuitton L, Tuxun T, Li J, Vuitton DA, Zhang W, McManus DP (2019) Echinococcosis: advances in the 21st Century. Clin Microbiol Rev 32(2):e00075-e118. https://doi.org/10.1128/CMR.00075-18

    Article  PubMed  PubMed Central  Google Scholar 

  • WHO (1996) Informal Working Group on Echinococcosis Guidelines for treatment of cystic and alveolar echinococcosis in humans. Bull World Health Organ 74:231–242

    Google Scholar 

  • Wintola OA, Afolayan AJ (2015) The antibacterial, phytochemicals and antioxidants evaluation of the root extracts of Hydnora africanaThunb. used as antidysenteric in Eastern Cape Province, South Africa. BMC Complement Altern Med 15:307

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ya-Min G, Wen-Jun Z, Shun-Yun Z, Xiu-Min H, Zheng-Guang X (2018) Surgical treatment strategy for complex hepatic echinococcosis: a review. Zhongguo Xue Xi Chong Bing Fang Zhi Za Zhi Chin 30(6):705–708. https://doi.org/10.16250/j.32.1374.2018169

    Article  Google Scholar 

Download references

Funding

None.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Javad Ghasemian Yadegari.

Ethics declarations

Conflict of interest

The authors declare no conflict of interest in this study.

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 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

Mahmoudvand, H., Al-Abodi, H.R., Zolfagharkhani, P. et al. Anti-helminthic effects and cellular mechanisms of Astragalus ecbatanus extract against Echinococcus granulosus protoscoleces. J Parasit Dis 46, 1047–1054 (2022). https://doi.org/10.1007/s12639-022-01517-y

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12639-022-01517-y

Keywords

Navigation