Abstract
Since the use of malachite green was banned, it is desirable to search for alternative drug to control Ichthyophthirius multifiliis infection. Moreover, route of administration which is easy to implement and less stressful to fish is important to treat infection of fish with this parasite. It is also important to enhance protective effect against Aeromonas hydrophila infection after parasitism by I. multifiliis. The present study evaluated the protective effect of diet supplemented with Artemisia annua against I. multifiliis and A. hydrophila infection after the parasitism. The results showed that oral administration with A. annua at a concentration of 20 g/kg feed for 45 days can provide strong protection against I. multifiliis infection. The incidence of infestation and mean number of trophonts on fish fins on day 3 post-challenge (15,000 theronts/fish) were significantly reduced compared with the control, and the survival rate of fish during 15-day period was also increased by nearly 30 %. But, this diet provided very limited protection against higher infection dose. Besides, this study demonstrated that this diet enhanced protective effect against A. hydrophila after the fish were infected with I. multifiliis. On the basis of the above results, oral administration with A. annua can be used as a potential strategy for control I. multifiliis infection and increasing fish survival after parasitism by I. multifiliis.
Similar content being viewed by others
References
Abdel-Hafez G, Lahnsteiner F, Mansour N (2014) Possibilities to control Ichthyophthirius multifiliis infestation with medicated feed in rainbow trout (Oncorhynchus mykiss) and chub (Leuciscus cephalus). Parasitol Res 113:1119–1126
Alderman D (1985) Malachite green: a review. J Fish Dis 8:289–298
Bhakuni RS, Jain DC, Sharma RP, Kumar S (2001) Secondary metabolites of Artemisia annua and their biological activity. Current Sci 80:35–48
Busch S, Dalsgaard I, Buchmann K (2003) Concomitant exposure of rainbow trout fry to Gyrodactylus derjavini and Flavobacterium psychrophilum: effects on infection and mortality of host. Vet Parasitol 117:117–122
Clayton GM, Price DJ (1988) Ichthyophthirius multifiliis: standardization of the infection-response model in Ameca splendens (Miller & Fitzsimons). J Fish Dis 11:371–377
Cusack R, Cone DK (1986) A review of parasites as vectors of viral and bacterial diseases of fish. J Fish Dis 9:169–171
Donno AD, Grassi T, Idolo A, Guido M, Papadia P, Caccioppola A, Villanova L, Merendino A, Bagordo F, Fanizzi FP (2012) First-time comparison of the in vitro antimalarial activity of Artemisia annua herbal tea and artemisinin. Trans R Soc Trop Med Hyg 106:696–700
Duke SO, Vaughn KC, Croom EM Jr, Elsohly HN (1987) Artemisinin, a constituent of annual wormwood (Artemisia annua), is a selective phytotoxin. Weed Sci 35:499–505
Emadi (2013) Phytochemistry of Artemisia annua. http://edd.behdasht.gov.ir/uploads/178_340_emadi.pdf. Accessed 4 Jun 2013
Evans JJ, Klesius PH, Pasnik DJ, Shoemaker CA (2007) Influence of natural Trichodina sp. parasitism on experimental Streptoccus iniae or Streptococcus agalactiae infection and survival of young channel catfish Ictalurus punctatus (Rafinesque). Aquat Res 38:664–667
Ferreira J, Janick J (2009) Annual wormwood (Artemisia annua L.). New Crop FactSHEET. www.hort.purdue.edu/newcrop/cropfactsheets/artemisia.pdf
Ferreira JFS, Ritchey KD, Cassida KL, Turner KE, Gonzalez JM (2006) Agrotechnological aspects of the anti-malarial plant Artemisia annua and its potential use in animal health in Appalachia. Revue des Régions Arides—Numéro spécial—Actes du séminaire international, les Plantes à Parfum, Aromatiques et Médicinales
Fu YW, Zhang QZ, Xu DH, Xia H, Cai XX, Wang B, Liang JH (2014a) Parasiticidal effects of Morus alba root bark extracts against Ichthyophthirius multifiliis infecting grass carp. Dis Aquat Organ 108:129–136
Fu YW, Zhang QZ, Xu DH, Liang JH, Wang B (2014b) Antiparasitic effect of cynatratoside-C from Cynanchum atratum against Ichthyophthirius multifiliis on grass carp. J Agric Food Chem 62:7183–7189
Hines RS, Spira DT (1973) Ichthyophthirius multifiliis (Fouquet) in the mirror carp, Cyprinus carpio L.I. Course of infection. J Fish Biol 5:385–392
Kumar S, Gupta SK, Singh P, Bajpai P, Gupta MM, Singh D, Gupta AK, Ram G, Shasany AK, Sharma S (2003) High yields of artemisinin by multi-harvest of Artemisia annua crops. Ind Crops Prod 19:77–90
Ling F, Wang JG, Liu QF, Li M, Ye LT, Gong XN (2010) Prevention of Ichthyophthirius multifiliis infestation in goldfish (Carassius auratus) by potassium ferrate (VI) treatment. Vet Parasitol 168:212–216
Ling F, Wang JG, Lu C, Wang GX, Lui YH, Gong XN (2012) Effects of aqueous extracts of Capsicum frutescens (Solanaceae) against of the fish ectoparasite Ichthyophthirius multifiliis. Parasitol Res 111:841–848
Ling F, Lu C, Tu X, Yi YL, Huang AG, Zhang QZ, Wang GX (2013) Antiprotozoal screening of traditional medicinal plants: evaluation of crude extract of Psoralea corylifolia against Ichthyophthirius multifiliis in goldfish. Parasitol Res 112:2331–2340
Luzardo-Álvarez A, Martínez-Mazagatos J, Santamarina-Fernández MT, Otero-Espinar FJ, Blanco-Méndez J (2003) Oral pharmacological treatments for ichthyophthiriosis of rainbow trout (Oncorhyncus mykiss). Aquaculture 220:15–25
Matthews RA (2005) Ichthyophthirius multifiliis Fouquet and ichthyophthiriosis in freshwater teleosts. Adv Parasitol 59:159–241
Naeem M, Idrees M, Singh M, Khan MMA, Moinuddin (2014) Chapter 3: Artemisia annua L.: a miraculous herb to cure Malaria. Artemisia annua—Pharmacology and Biotechnology, T. Aftab et al. (eds.). DOI: 10.1007/978-3-642-41027-7_2. Springer-Verlag Berlin Heidelberg
Nielsen ME, Høi L, Schmidt AS, Qian D, Shimada T, Shen JY, Larsen JL (2001) Is Aeromonas hydrophila the dominant motile Aeromonas species that causes disease outbreaks in aquaculture production in the Zhejiang Province of China? Dis Aquat Organ 46:23–29
Picón-Camacho SM, Marcos-Lopez M, Bron JE, Shinn AP (2012) An assessment of the use of drug and non-drug interventions in the treatment of Ichthyophthirius multifiliis Fouquet, 1876, a protozoan parasite of freshwater fish. Parasitology 139:149–190
Plumb JA (1994) Health maintenance and principal microbial diseases of cultured fishes. CRC Press, Boca Raton, 328 pp
Rogers WA, Gaines JL (1975) Lesions of protozoan diseases in fish. In: Ribelin WE, Migaki G (eds) The pathology of fishes. University of Wisconsin Press, Madison, pp 117–141
Sadiq A, Hayat QM, Ashraf M (2014) Chapter 2: Ethnopharmacology of Artemisia annua L.: a review. Artemisia annua—Pharmacology and Biotechnology, T. Aftab et al. (eds.). DOI: 10.1007/978-3-642-41027-7_2. Springer-Verlag Berlin Heidelberg
Schlenk D, Gollon JL, Griffin BR (1998) Efficacy of copper sulfate in the treatment of ichthyophthiriosis in channel catfish. J Aquat Anim Health 10:390–396
Schmahl G, Ruider S, Mehlhorn H, Schmidt H, Ritter G (1992) Treatment of fish parasites: 9. Effects of a medicated food containing malachite green on Ichthyophthirius multifiliis Fouquet, 1876 (Hymenostomatida, Ciliophora) in ornamental fish. Parasitol Res 78:183–192
Schmahl G, Schmidt H, Ritter G (1996) The control of ichthyophthiriasis by a medicated food containing quinine: efficacy tests and ultrastructural investigations. Parasitol Res 82:697–705
Shinn AP, Picón-Camacho SM, Bron JE, Conway D, Yoon GH, Guo FC, Taylor NGH (2012) The anti-protozoal activity of bronopol on the key life-stages of Ichthyophthirius multifiliis Fouquet, 1876 (Ciliphora). Vet Parasitol 186:229–236
Song KG, Ling F, Huang AG, Dong WJ, Liu GL, Jiang C, Zhang QZ, Wang GX (2015) In vitro and in vivo assessment of the effect of antiprotozoal compounds isolated from Psoralea corylifolia against Ichthyophthirius multifiliis in fish. Int J Parasitol: Drug Drug Resist 5:58–64
Straus DL, Griffin BR (2001) Prevention of an initial infestation of Ichthyophthirius multifiliis in channel catfish and blue tilapia by potassium permanganate treatment. N Am J Aquacult 63:11–16
Tayebe S, Mehrnaz K, Khosro P, Tahere H (2012) Morphological evaluation of hairy roots induced in Artemisia annua L. and investigating elicitation effects on the hairy roots biomass production. Int J Agric: Res Rev 2:1005–1013 (Special issue)
Willcox M (2009) Artemisia species: from traditional medicines to modern antimalarials and back again. J Altern Complement Med 15:101–109
Xu DH, Shoemaker C, Klesius P (2007) Evaluation of the link between gyrodactylosis and streptococcosis of Nile tilapia, Oreochromis niloticus. J Fish Dis 30:233–238
Xu DH, Shoemaker C, Klesius P (2009) Enhanced mortality in Nile tilapia, Oreochromis niloticus (L.) following coinfections with ichthyophthiriasis and streptococcosis. Dis Aquat Organ 85:187–192
Xu DH, Pridgeon JW, Klesius PH, Shoemaker CA (2012a) Parasitism by protozoan Ichthyophthirius multifiliis enhanced invasion of Aeromonas hydrophila in tissues of channel catfish. Vet Parasotol 184:101–107
Xu DH, Shoemaker CA, Martins ML, Prodgeon JW, Klesius PH (2012b) Enhanced susceptibility of channel catfish to the bacterium Edwardsiella ictaluri after parasitism by Ichthyophthirius multifiliis. Vet Microbiol 158:216–219
Xu DH, Shoemaker CA, Lafrentz BR (2014) Enhanced susceptibility of hybrid tilapia to Flavobacterium columnare after parasitism by Ichthyophthirius multifiliis. Aquaculture 430:44–49
Yao JY, Zhou ZM, Li XL, Yin WL, Ru HS, Pan XY, Hao GJ, Xu Y, Shen JY (2011) Antiparasitic efficacy of dihydrosanguinarine and dihydrochelerythrine from Macleaya microcarpa against Ichthyophthirius multifiliis in richadsin (Squaliobarbus curriculus). Vet Parasitol 183:8–13
Zhang C, Ling F, Chi C, Wang GX (2013) Effects of praziquantel and sanguinarine on expression of immune genes and susceptibility to Aeromonas hydrophila in goldfish (Carassius auratus) infected with Dactylogyrus intermedius. Fish Shellfish Immunol 35:1301–1308
Acknowledgments
Financial support for this study was provided by the National Natural Science Foundation of China (NSFC) under Grant 31202035 and Specialized Research Fund for the Doctoral Program of Higher Education (SRFDP) under Grant 20120204120004.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Wu, Z., Ling, F., Song, C. et al. Effects of oral administration of whole plants of Artemisia annua on Ichthyophthirius multifiliis and Aeromonas hydrophila after parasitism by I. multifiliis . Parasitol Res 116, 91–97 (2017). https://doi.org/10.1007/s00436-016-5265-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00436-016-5265-1