Skip to main content

Advertisement

SpringerLink
Log in

In vivo anthelmintic effect of flavonol rhamnosides from Dryopteris crassirhizoma against Dactylogyrus intermedius in goldfish (Carassius auratus)

  • Original Paper
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

The purpose of the present study was to assess the anthelmintic property of plant-derived polyphenolic compounds extracted and isolated from Dryopteris crassirhizoma against Dactylogyrus intermedius in goldfish. The active ethyl acetate extract was loaded on an open silica gel column and eluted with chloroform–methanol. According to 1H-nuclear magnetic resonance (NMR), 13C-NMR, and mass spectral data, the structures of three purified compounds were identified as protocatechuic acid, sutchuenoside A, and kaempferitrin. Among these compounds, sutchuenoside A and kaempferitrin were observed to be effective with median effective concentration (EC50) of 3.01 and 2.71 mg L−1, respectively. The alterations in the tegument of the parasites treated with isolated compound were examined using scanning electron microscopes. Ultrastructural micrographs revealed shrinkage of body surface, dense tegumental folds, and disheveled protuberances. The structural deformities in the treated parasites were indicative of an efficient anthelmintic activity of the isolated compound kaempferitrin. In addition, the 48-h median lethal concentration for sutchuenoside A and kaempferitrin against goldfish were 12.03- and 11.98-fold higher than corresponding EC50. The present results showed that ethyl acetate extract of D. crassirhizoma may be considered as a potent source, and sutchuenoside A and kaempferitrin as new natural parasitic agents against D. intermedius.

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

Similar content being viewed by others

References

  • Alonso-Castro AJ et al (2013) Kaempferitrin induces apoptosis via intrinsic pathway in HeLa cells and exerts antitumor effects. J Ethnopharmacol 145(2):476–489

    Article  PubMed  CAS  Google Scholar 

  • Alvarez-Pellitero P (2004) Report about fish parasitic diseases. In: Alvarez-Pellitero P, Barja JL, Basurco B, Berthe F, Toranzo AE (eds) Mediterranean aquaculture diagnostic laboratories. CIHEAM/FAO, Zaragoza, Spain, pp 123–124

    Google Scholar 

  • Banerjee RD, Sen SP (1980) Antibiotic activity of pteridophytes. Econ Bot 34(3):284–298

    Article  Google Scholar 

  • Barrau E, Fabre N, Fouraste I, Hoste H (2005) Effect of bioactive compounds from Sainfoin (Onobrychis viciifolia Scop.) on the in vitro larval migration of Haemonchus contortus: role of tannins and flavonol glycosides. Parasitology 131(4):531–538

    Article  PubMed  CAS  Google Scholar 

  • Beecher GR (2003) Overview of dietary flavonoids: nomenclature, occurrence, and intake. J Nutr 133(10):3248S–3254S

    PubMed  CAS  Google Scholar 

  • Buchmann K, Slotved HC, Dana D (1993) Epidemiology of gill parasite infections in Cyprinus carpio in Indonesia and possible control methods. Aquaculture 118(1–2):9–21

    Article  CAS  Google Scholar 

  • Burka JF, Hammell KL, Horsberg TE, Johnson GR, Rainnie DJ, Speare DJ (1997) Drugs in salmonid aquaculture: a review. J Vet Pharmacol Ther 20(5):333–349

    Article  PubMed  CAS  Google Scholar 

  • Calderón-Montaño JM, Burgos-Morón E, Pérez-Guerrero C, López-Lázaro M (2011) A review on the dietary flavonoid kaempferol. Mini Rev Med Chem 11(4):298–344

    Article  PubMed  Google Scholar 

  • Chang SH et al (2010) Dryopteris crassirhizoma has anticancer effects through both extrinsic and intrinsic apoptotic pathways and G0/G1 phase arrest in human prostate cancer cells. J Ethnopharmacol 130(2):248–254

    Article  PubMed  CAS  Google Scholar 

  • Chansue N, Tangtrongpiros J (2005) Effect of dried Indian almond leaf (Terminalia catappa) on monogenean parasite of gold fish (Carassius auratus). Wetchasan Sattawaphaet 35

  • Chaturvedula VSP, Prakash I (2011) Kaempferol glycosides from Siraitia grosvenorii. J Chem Pharm Res 3(6):799–804

    CAS  Google Scholar 

  • Commission CP (2005) The Pharmacopeia of the People’s Republic of China. Chemical Industry Press, Beijing

    Google Scholar 

  • Chitwood DJ (2002) Phytochemical-based strategies for nematode control. Annu Rev Phytopathol 40(1):221–249

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

  • de Sousa E et al (2004) Hypoglycemic effect and antioxidant potential of kaempferol-3, 7-O-(α)-dirhamnoside from Bauhinia forficata leaves. J Nat Prod 67(5):829–832

    Article  PubMed  Google Scholar 

  • Del Carmen J-VM, Josabad Alonso-Castro A, García-Carrancá A (2013) Kaempferitrin induces immunostimulatory effects in vitro. J Ethnopharmacol 148(1):337–340

    Article  Google Scholar 

  • Dennison C, Lawler AT, Kohzuma T (2001) Unusual properties of plastocyanin from the fern Dryopteris crassirhizoma. Biochemistry 41(2):552–560

    Article  Google Scholar 

  • Ekanem AP, Brisibe EA (2010) Effects of ethanol extract of Artemisia annua L. against monogenean parasites of Heterobranchus longifilis. Parasitol Res 106(5):1135–1139

    Article  PubMed  Google Scholar 

  • Ellis JE (1974) A review of the literature on the use of Masoten in fisheries. Report No. FWS-LR-74–13, US Fish and Wildlife Service, Division of Popular Resources Regulation.

  • FAO (2010) The state of world fisheries and aquaculture. Food and Agriculture Organization of the United Nations. Rome, Italy

    Google Scholar 

  • Finney DJ (1971) Probit Analysis, 3rd edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Flamini G, Antognoli E, Morelli I (2001) Two flavonoids and other compounds from the aerial parts of Centaurea bracteata from Italy. Phytochemistry 57(4):559–564

    Article  PubMed  CAS  Google Scholar 

  • Gao Z et al (2008) Phytochemical investigation of the rhizomes of Dryopteris crassirhizoma. Phytochem Lett 1(4):188–190

    Article  CAS  Google Scholar 

  • Gohara AA, Elmazar M (1997) Isolation of hypotensive flavonoids from Chenopodium sp. growing in Egypt. Phytother Res 11(8):564–567

    Article  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55(6):481–504

    Article  PubMed  CAS  Google Scholar 

  • Johnson JL, Rupasinghe SG, Stefani F, Schuler MA, Gonzalez de Mejia E (2011) Citrus flavonoids luteolin, apigenin, and quercetin inhibit glycogen synthase kinase-3β enzymatic activity by lowering the interaction energy within the binding cavity. J Med Food 14(4):325–333

    Article  PubMed  CAS  Google Scholar 

  • Kapadia GJ, Tokuda H, Konoshima T et al (1996) Anti-tumor promoting activity of Dryopteris phlorophenone derivatives. Cancer Lett 105(2):161–165

    Article  PubMed  CAS  Google Scholar 

  • Kar PK, Tandon V, Saha N (2002) Anthelmintic efficacy of Flemingia vestita: genistein-induced effect on the activity of nitric oxide synthase and nitric oxide in the trematode parasite, Fasciolopsis buski. Parasitol Int 51(3):249–257

    Article  PubMed  Google Scholar 

  • Klinger R, Floyd RF (2009) Introduction to freshwater fish parasites. Document CIR716. Institute of Food and Agricultural Science. University of Florida, Florida

    Google Scholar 

  • Kritsky DC, Heckmann R (2002) Species of Dactylogyrus (Monogenoidea: Dactylogyridae) and Trichodina mutabilis (Ciliata) infesting Koi carp, Cyprinus carpio, during mass mortality at a commercial rearing facility in Utah, USA. Comp Parasitol 69(2):217–218

    Article  Google Scholar 

  • Kundu S, Roy S, Lyndem LM (2012) Cassia alata L: potential role as anthelmintic agent against Hymenolepis diminuta. Parasitol Res 111(3):1187–1192

    Article  PubMed  Google Scholar 

  • Kwon YS et al (2004) Modulation of suppressive activity of lipopolysaccharide-induced nitric oxide production by glycosidation of flavonoids. Arch Pharm Res 27(7):751–756

    Article  PubMed  CAS  Google Scholar 

  • Lee HB, Kim JC, Lee SM (2009) Antibacterial activity of two phloroglucinols, flavaspidic acids AB and PB, from Dryopteris crassirhizoma. Arch Pharm Res 32(5):655–659

    Article  PubMed  CAS  Google Scholar 

  • Lee JS, Miyashiro H, Nakamura N, Hattori M (2008) Two new triterpenes from the rhizome of Dryopteris crassirhizoma, and inhibitory activities of its constituents on human immunodeficiency virus-1 protease. Chem Pharm Bull 56(5):711–714

    Article  PubMed  CAS  Google Scholar 

  • Lee SM, Na MK, An RB, Min BS, Lee HK (2003) Antioxidant activity of two phloroglucinol derivatives from Dryopteris crassirhizoma (Pharmacognosy). Biol Pharm Bull 26(9):1354–1356

    Article  PubMed  CAS  Google Scholar 

  • Lim Y, Kim I, Seo J (2007) In vitro activity of kaempferol isolated from the Impatiens balsamina alone and in combination with erythromycin or clindamycin against Propionibacterium acnes. J Microbiol 45(5):473–477

    PubMed  CAS  Google Scholar 

  • Liu YT, Wang F, Wang GX, Han J, Wang Y, Wang YH (2010) In vivo anthelmintic activity of crude extracts of Radix angelicae pubescentis, Fructus bruceae, Caulis spatholobi, Semen aesculi, and Semen pharbitidis against Dactylogyrus intermedius (Monogenean) in goldfish (Carassius auratus). Parasitol Res 106(5):1233–1239

    Article  PubMed  Google Scholar 

  • Lu C, Zhang HY, Ji J, Wang GX (2012) In vivo anthelmintic activity of Dryopteris crassirhizoma, Kochia scoparia, and Polygala tenuifolia against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus). Parasitol Res 110(3):1085–1090

    Article  PubMed  Google Scholar 

  • Magalhaes LG et al (2010) In vitro schistosomicidal effects of some phloroglucinol derivatives from Dryopteris sp. against Schistosoma mansoni adult worms. Parasitol Res 106(2):395–401

    Article  PubMed  Google Scholar 

  • Martin RJ, Robertson AP, Bjorn H (1997) Target sites of anthelmintics. Parasitology 114(07):111–124

    Google Scholar 

  • Mazzio EA, Soliman KF (2009) In vitro screening for the tumoricidal properties of international medicinal herbs. Phytother Res 23(3):385–398

    Article  PubMed  CAS  Google Scholar 

  • Min BS, Tomiyama M, Ma CM, Nakamura N, Hattori M (2001) Kaempferol acetylrhamnosides from the rhizome of Dryopteris crassirhizoma and their inhibitory effects on three different activities of human immunodeficiency virus-1 reverse transcriptase. Chem Pharm Bull 49(5):546–550

    Article  PubMed  CAS  Google Scholar 

  • Mizuno M, Iinuma M, Tanaka T, Yamamoto H, Tu ZB (1991) Sutchuenoside A: a new kaempferol glycoside from the aerial parts of Epimedium sutchuenense. J Nat Prod 54(5):1427–1429

    Article  CAS  Google Scholar 

  • Na M et al (2006) Fatty acid synthase inhibitory activity of acylphloroglucinols isolated from Dryopteris crassirhizoma. Bioorg Med Chem Lett 16(18):4738–4742

    Article  PubMed  CAS  Google Scholar 

  • Ojo KK et al (2008) Glycogen synthase kinase 3 is a potential drug target for African trypanosomiasis therapy. Antimicrob Agents Chemother 52(10):3710–3717

    Article  PubMed  CAS  Google Scholar 

  • Pletneva EV, Fulton DB, Kohzuma T, Kostić NM (2000) Protein docking and gated electron-transfer reactions between zinc cytochrome c and the new plastocyanin from the fern Dryopteris crassirhizoma. Direct kinetic evidence for multiple binary complexes. J Am Chem Soc 122(6):1034–1046

    Article  CAS  Google Scholar 

  • Reed PA, Francis-Floyd R, Klinger RC (2009) Monogenean parasites of fish. http://edis.ifas.ufl.edu/FA033. Accessed 17 May 2009

  • Schmahl G (1993) Treatment of fish parasites. 10. Effects of a new triazine derivative, HOE 092 V, on Monogenea: a light and transmission electron microscopy study. Parasitol Res 79(7):559

    Article  PubMed  CAS  Google Scholar 

  • Schmahl G, Mehlhorn H (1985) Treatment of fish parasites: 1. Praziquantel effective against Monogenea (Dactylogyrus vastator, Dactylogyrus extensus, Diplozoon paradoxum). Z Parasitenkd 71(6):727–737

    Article  PubMed  CAS  Google Scholar 

  • Schmahl G, Mehlhorn H, Haberkorn A (1988) Sym. triazinone (toltrazuril) effective against fish-parasitizing Monogenea. Parasitol Res 75(1):67–68

    Article  PubMed  CAS  Google Scholar 

  • Shiojima J, Suzuki M, Matsumura T, Ageta H (1994) Fern constituent: a new triterpenoid hydocarbon, trisnorhopane, isolated from the leaves of Dryopteris crassirhizoma and Gleichenia japonica. Chem Pharm Bull 42(2):377–378

    Article  CAS  Google Scholar 

  • Thompson D, Geary T (1995) The structure and function of helminth surfaces. In: Marr J (ed) Biochemistry and molecular biology of parasites. Academic, New York, pp 203–232

    Chapter  Google Scholar 

  • Tonguthai K (1997) Control of freshwater fish parasites: a Southeast Asian perspective. Int J Parasitol 27(10):1185–1191

    Article  PubMed  CAS  Google Scholar 

  • Trumbeckaite S, Bernatoniene J, Majiene D, Jakštas V, Savickas A, Toleikis A (2006) The effect of flavonoids on rat heart mitochondrial function. Biomed Pharmacother 60(5):245–248

    Article  PubMed  CAS  Google Scholar 

  • Vishnu Prasad CN, Suma Mohan S, Banerji A, Gopalakrishnapillai A (2009) Kaempferitrin inhibits GLUT4 translocation and glucose uptake in 3T3-L1 adipocytes. Biochem Biophys Res Commun 380(1):39–43

    Article  PubMed  CAS  Google Scholar 

  • Wang G, Zhou Z, Cheng C, Yao J, Yang Z (2008) Osthol and isopimpinellin from Fructus cnidii for the control of Dactylogyrus intermedius in Carassius auratus. Vet Parasitol 158(1–2):144–151

    Article  PubMed  CAS  Google Scholar 

  • Widén C, Lounasmaa M, Sarvela J (1975) Phloroglucinol derivatives of Dryopteris crassirhizoma from Japan. Acta Chem Scand 29:859–862

    Article  Google Scholar 

  • Wu MJ, Zhang Y, Zhang HY, Zhao TZ (2012) NMR numerical analysis of sutchuenoside A. J Zhengzhou Univ (Eng Sci) 33(1):67–80

    Google Scholar 

  • Xu YC et al (2007) Structure-activity relationships of flavonoids for vascular relaxation in porcine coronary artery. Phytochemistry 68(8):1179–1188

    Article  PubMed  CAS  Google Scholar 

  • Yuan XH, Chen W (2012) Use of veterinary medicines in Chinese aquaculture: current status. In: Bondad-Reantaso MG, Arthur JR, Subasinghe RP (eds) Improving biosecurity through prudent and responsible use of veterinary medicines in aquatic food production. FAO Fisheries and Aquaculture Technical Paper No. 547, Rome, pp 51-67

  • Zahir AA, Rahuman AA, Bagavan A, Geetha K, Kamaraj C, Elango G (2012) Evaluation of medicinal plant extracts and isolated compound epicatechin from Ricinus communis against Paramphistomum cervi. Parasitol Res 111(4):1629–1635

    Article  PubMed  Google Scholar 

  • Zhang S, Zhao H, Zhang Q, Lin Y, Gao Z (2012) Evaluation of antioxidant activity of flavonoids and phloroglucinols from Guanzhong. Planta Med 78(05):53

    Google Scholar 

  • Wu ZF, Zhu B, Wang Y, Lu C, Wang GX (2011) In vivo evaluation of anthelmintic potential of medicinal plant extracts against Dactylogyrus intermedius (Monogenea) in goldfish (Carassius auratus). Parasitol Res 108(6):1557–1563

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported by the National High Technology Research and Development Program of China (also called 863 Program) under grant 2011AA10A216.

Author information

Authors and Affiliations

  1. Northwest A&F University, Yangling, Shaanxi, 712100, People’s Republic of China

    Bing Jiang, Cheng Chi & Gao-xue Wang

  2. Engineering Research Center of Tropical and Subtropical Aquatic Ecological Engineering Minister of Education, Key Laboratory of Eutrophication and Red Tide Prevention of Guangdong Higher Education Institutes, Institute of Hydrobiology, Jinan University, Guangzhou, 510632, People’s Republic of China

    Yao-wu Fu & Qi-zhong Zhang

Authors
  1. Bing Jiang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cheng Chi
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yao-wu Fu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Qi-zhong Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Gao-xue Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Qi-zhong Zhang or Gao-xue Wang.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Jiang, B., Chi, C., Fu, Yw. et al. In vivo anthelmintic effect of flavonol rhamnosides from Dryopteris crassirhizoma against Dactylogyrus intermedius in goldfish (Carassius auratus). Parasitol Res 112, 4097–4104 (2013). https://doi.org/10.1007/s00436-013-3600-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-013-3600-3

Keywords

Search

Navigation