Skip to main content

Advertisement

SpringerLink
Log in

Towards identifying novel anti-Eimeria agents: trace elements, vitamins, and plant-based natural products

  • Review
  • Published:
Parasitology Research Aims and scope Submit manuscript

Abstract

Eimeriosis, a widespread infectious disease of livestock, is caused by coccidian protozoans of the genus Eimeria. These obligate intracellular parasites strike the digestive tract of their hosts and give rise to enormous economic losses, particularly in poultry, ruminants including cattle, and rabbit farming. Vaccination, though a rational prophylactic measure, has not yet been as successful as initially thought. Numerous broad-spectrum anti-coccidial drugs are currently in use for treatment and prophylactic control of eimeriosis. However, increasing concerns about parasite resistance, consumer health, and environmental safety of the commercial drugs warrant efforts to search for novel agents with anti-Eimeria activity. This review summarizes current approaches to prevent and treat eimeriosis such as vaccination and commercial drugs, as well as recent attempts to use dietary antioxidants as novel anti-Eimeria agents. In particular, the trace elements selenium and zinc, the vitamins A and E, and natural products extracted from garlic, barberry, pomegranate, sweet wormwood, and other plants are discussed. Several of these novel anti-Eimeria agents exhibit a protective role against oxidative stress that occurs not only in the intestine of Eimeria-infected animals, but also in their non-parasitized tissues, in particular, in the first-pass organ liver. Currently, it appears to be promising to identify safe combinations of low-cost natural products with high anti-Eimeria efficacy for a potential use as feed supplementation in animal farming.

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

Similar content being viewed by others

References

  • Abdel-Ghaffar F, Semmler M, Al-Rasheid KA, Strassen B, Fischer K, Aksu G, Klimpel S, Mehlhorn H (2010) The effects of different plant extracts on intestinal cestodes and on trematodes. Parasitol Res 108:979–984

    PubMed  Google Scholar 

  • Abdel-Moneim AE (2012) Evaluating the potential role of pomegranate peel in aluminum-induced oxidative stress and histopathological alterations in brain of female rats. Biol Trace Elem Res 150:328–336

    PubMed  Google Scholar 

  • Al-Mathal EM, Alsalem AM (2012) Pomegranate (Punica granatum) peel is effective in a murine model of experimental Cryptosporidium parvum. Exp Parasitol 131:350–357

    PubMed  Google Scholar 

  • Alnassan AA, Shehata AA, Kotsch M, Schrödl W, Krüger M, Daugschies A, Bangoura B (2013) Efficacy of early treatment with toltrazuril in prevention of coccidiosis and necrotic enteritis in chickens. Avian Pathol 42:482–490

    PubMed  CAS  Google Scholar 

  • Alnassan AA, Kotsch M, Shehata AA, Krüger M, Daugschies A, Bangoura B (2014) Necrotic enteritis in chickens: development of a straightforward disease model system. Vet Rec 174:555

    PubMed  CAS  Google Scholar 

  • Al-Quraishy S, Delic D, Sies H, Wunderlich F, Abdel-Baki AA, Dkhil MA (2011) Differential miRNA expression in the mouse jejunum during garlic treatment of Eimeria papillata infections. Parasitol Res 109:387–394

    PubMed  Google Scholar 

  • Al-Quraishy S, Metwaly MS, Dkhil M, Abdel-Baki AA, Wunderlich F (2012) Liver response of rabbits to Eimeria coecicola infections. Parasitol Res 110:901–911

    PubMed  Google Scholar 

  • Al-Quraishy S, Sherif NR, Metwaly MS, Dkhil M (2014) Berberine-induced amelioration of the pathological changes in nutrient’s homeostasis during murine intestinal Eimeria papillata infection. Pakistan J Zool 46:437–445

    CAS  Google Scholar 

  • Al-Taher AY (2008) Possible anti-diarrhoeal effect of the date palm (Phoenix dactylifera L) spathe aqueous extract in rats. Sci J King Feisal Univ 9:131–138

    Google Scholar 

  • Alzoreky NS, Nakahara K (2003) Antibacterial activity of extracts from some edible plants commonly consumed in Asia. Int J Food Microbiol 80:223–230

    PubMed  CAS  Google Scholar 

  • An RB, Oh H, Kim YC (2005) Phenolic constituents of Galla rhois with hepatoprotective effects on tacrine- and nitrofurantoin-induced cytotoxicity in HepG2 cells. Biol Pharm Bull 28:2155–2157

    PubMed  CAS  Google Scholar 

  • Bafundo KW, Baker DH, Fitzgerald PR (1984) Zinc utilization in the chick as influenced by dietary concentrations of calcium and phytate and by Eimeria acervulina infection. Poult Sci 63:2430–2437

    PubMed  CAS  Google Scholar 

  • Bala S, Petrasek J, Mundkur S, Catalano D, Levin I, Ward J, Alao H, Kodys K, Szabo G (2012) Circulating microRNAs in exosomes indicate hepatocyte injury and inflammation in alcoholic, drug-induced, and inflammatory liver diseases. Hepatology 56:1946–1957

    PubMed  PubMed Central  CAS  Google Scholar 

  • Baliga MS, Baliga BR, Kandathil SM, Bhat HP, Vayalil PK (2011) A review of the chemistry and pharmacology of the date fruits (Phoenix dactylifera L.). Food Res Int 44:1812–1822

    CAS  Google Scholar 

  • Barik S (2006) Immunophilins: for the love of proteins. Cell Mol Life Sci 63:2889–2900

    PubMed  CAS  Google Scholar 

  • Bell A, Monghan P, Page AP (2006) Peptidyl-prolyl cis-trans isomeares (immunophilins) and their roles in parasite chemistry, host–parasite interaction and anti-parasitic drug action. Intern J Parasitol 36:261–276

    CAS  Google Scholar 

  • Bierbaum S (2009) Das Cyclophilin EtCyp 20.5 aus Eimeria tenella als Rezeptor für das Antikokzidium Toltrazuril. Inaugural-Dissertation, Math.-Nat. Faculty, Heinrich-Heine-University, Duesseldorf, Germany

  • Blake DP, Tomley FM (2014) Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol 30:12–19

    PubMed  Google Scholar 

  • Calzada F, Yepez-Mulia L, Aguilar A (2006) In vitro susceptibility of Entamoeba histolytica and Giardia lamblia to plants used in Mexican traditional medicine for the treatment of gastrointestinal disorders. J Ethnopharmacol 108:367–370

    PubMed  Google Scholar 

  • Chapman HD (2001) Use of anticoccidial drugs in broiler chickens in the USA: analysis for the years 1995 to1999. Poult Sci 80:572–580

    PubMed  CAS  Google Scholar 

  • Chapman HD (2014) Milestones in avian coccidiosis research: a review. Poult Sci 93:501–511

    PubMed  CAS  Google Scholar 

  • Chew BP (1995) Antioxidant vitamins affect food animal immunity and health. J Nutr 125:18045–18085

    Google Scholar 

  • Chew BP, Park JS (2004) Carotenoid action on the immune response. J Nutr 134:257–261

    Google Scholar 

  • Chowdury AK, Ahson M, Nazrul-Islam SK, Ahmed ZU (1991) Efficacy of aqueous extract of garlic and allicin in experimental shigellosis in rabbits. Indian J Med Res 93:33–36

    Google Scholar 

  • Christaki E, Florou-Paneri P, Giannenas I, PaPazahariadou M, Botsoglou NA (2004) Effect of mixture of herbal extracts on broiler chickens infected with Eimeria tenella. Anim Res 53:137–144

    CAS  Google Scholar 

  • Chung LY (2006) The antioxidant properties of garlic compounds: allyl csyteine, allinin, allicin, allyl disulfide. J Med Food 9:205–213

    PubMed  CAS  Google Scholar 

  • Colnago GL, Jensen LS, Long PL (1984) Effect of selenium and vitamin E on the development of immunity to coccidiosis in chickens. Poult Sci 63:1136–1143

    PubMed  CAS  Google Scholar 

  • Dalloul RA, Lillehoj HS (2005) Recent advances in immunomodulation and vaccination strategies against coccidiosis. Avian Dis 49:1–8

    PubMed  Google Scholar 

  • Dalloul R, Lillehoj H (2006) Poultry coccidiosis: recent advancements in control measures and vaccine development. Exp Rev Vaccines 5:143–163

    CAS  Google Scholar 

  • Dalloul RA, Lillehoj HS, Shellern TA, Doerr JA (2002) Effect of vitamin a deficiency on host intestinal immune response to Eimeria acervulina in broiler chickens. Poult Sci 81:1509–1515

    PubMed  CAS  Google Scholar 

  • Dalloul RA, Lillehoj HS, Shellern TA, Doerr JA (2003) Intestinal immunomodulation by vitamin A deficiency and Lactobacillus-based probiotic in Eimeria acervulina infected chickens broiler. Avain Dis 47:1313–1320

    Google Scholar 

  • Darius AK, Mehlhorn H, Heydorn AO (2004) Effects of toltrazuril and ponazuril on Hammondia heydorni (syn. Neospora caninum) infections in mice. Parasitol Res 92:520–522

    PubMed  Google Scholar 

  • Daugschies A, Najdrowski M (2005) Eimeriosis in cattle: current understanding. J Vet Med B Infect Dis Vet Public Health 52:417–427

    PubMed  CAS  Google Scholar 

  • Dell’Agli M, Galli G, Corbett Y, Taramelli D, Lucantoni L, Habluetzel A, Maschi O, Caruso D, Giavarini F, Romeo S, Bhattacharya D, Bosisio E (2009) Antiplasmodial activity of Punica granatum L. fruit rind. J Ethnopharmacol 125:279–285

    PubMed  Google Scholar 

  • Dkhil MA (2013) Anti-coccidial, anthelmintic and antioxidant activities of pomegranate (Punica granatum) peel extract. Parasitol Res 112:2639–2646

    PubMed  Google Scholar 

  • Dkhil MA (2014) Role of berberine in ameliorating Schistosoma mansoni-induced hepatic injury in mice. Biol Res 47:8

    PubMed  PubMed Central  Google Scholar 

  • Dkhil M, Abdel-Maksoud MA, Al-Quraishy S, Abdel-Baki AA, Wunderlich F (2012) Gene expression in rabbit appendides infected with Eimeria coecicola. Vet Parasitol 186:222–228

    PubMed  CAS  Google Scholar 

  • Dkhil MA, Al-Quraishy S, Abdel Moneim AE, Delic D (2013a) Protective effect of Azadirachta indica extract against Eimeria papillata-induced coccidiosis. Parasitol Res 112:101–106

    PubMed  Google Scholar 

  • Dkhil MA, Al-Quraishy S, Abdel-Baki AA, Delic D, Wunderlich F (2013b) Eimeria coecicola: spleen response of Oryctolagus cuniculus. Exp Parasitol 133:137–143

    PubMed  CAS  Google Scholar 

  • Dkhil MA, Abdel-Baki AA, Wunderlich F, Sies H, Al-Quraishy S (2014) Dietary selenium affects intestinal development of Eimeria papillata in mice. Parasitol Res 113:267–274

    PubMed  Google Scholar 

  • Drăgan L, Györke A, Ferreira JF, Pop IA, Dunca I, Drăgan M, Mircean V, Dan I, Cozma V (2014) Effects of Artemisia annua and Foeniculum vulgare on chickens highly infected with Eimeria tenella (phylum Apicomplexa). Acta Vet Scand 56:22

    PubMed  PubMed Central  Google Scholar 

  • Drucker C, Gewiese J, Malchow S, Scheller J, Rose-John S (2010) Impact of interleukin-6 classic- and trans-signaling on liver damage and regeneration. J Autoimmun 34:29–37

    PubMed  CAS  Google Scholar 

  • Duraka A, Özturk HS, Olcay E, Guven C (2002) Effects of garlic extract supplementation on blood lipid and antioxidant parameters and atherosclerotic plaque formation process in cholesterol-fed rabbits. J Herbal Pharmacother 2:19–32

    Google Scholar 

  • EFSA (European Food Safety Authority) (2014) Scientific opinion on the safety and efficacy of dl-selenomethionine as a feed additive for all animal species. EFSA Journal 12:3567–3586

    Google Scholar 

  • Elavarasu S, Abinaya P, Elanchezhiyan S, Thangakumaran VK, Naziya KB (2012) Evaluation of anti-plaque microbial activity of Azadirachta indica (neem oil) in vitro: a pilot study. J Pharm Bioallied Sci 4:S394–S396

    PubMed  PubMed Central  Google Scholar 

  • Ezz-Din D, Gabry MS, Farrag AH, Abdel Moneim AE (2011) Physiological and histological impact of Azadirachta indica (neem) leaves extract in a rat model of cisplatin-induced hepato and nephrotoxicity. J Med Plants Res 5:5499–5506

    CAS  Google Scholar 

  • Fabbri M, Paone A, Calore F, Galli R, Gaudio E, Santhanam R, Lovat F, Fadda P, Mao C, Nuovo GJ, Zanesi N, Crawford M, Ozer GH, Wernicke D, Alder H, Caligiuri MA, Nana-Sinkam P, Perrotti D, Croce CM (2012) MicroRNAs bind to Toll-like receptors to induce prometastatic inflammatory response. Proc Natl Acad Sci U S A 109:E2110–E2116

    PubMed  PubMed Central  CAS  Google Scholar 

  • Fernandes RM, Rodrigues MLA, Borba HR, Fernandes MZCM, de Amorim A (2004a) Ausência da atividade anti-helmíntica de plantas em frangos de corte naturalmente infectados com Heterakis gallinarum (Schranck,1788) Madsen, 1949. Cienc Rural 34:1629–1682

    Google Scholar 

  • Fernandes RM, Rodrigues MLA, Borba HR, Fernandes MZCM, de Amorim A (2004b) Ausência da atividade anti-helmíntica de plantas em frangos de corte naturalmente infectados com Heterakis gallinarum (Schranck, 1788) Madsen, 1949. Ciencia Rural 34:1629–1682

    Google Scholar 

  • Ferreira JFS, Peaden P, Keiser J (2011) In vitro trematocidal effects of crude alcoholic extracts of Artemisia annua, A absinthium, Asimina triloba, and Fumaria officinalis: trematocidal plant alcoholic extracts. Parasitol Res 109:1585–1592

    PubMed  Google Scholar 

  • Fleischauer AT, Poole CH, Arab L (2000) Garlic consumption and cancer prevention: meta-analyses of colorectal and stomach cancers. Am J Clin Nutr 72:1047–1052

    PubMed  CAS  Google Scholar 

  • Fossum O, Jansson DS, Etterlin PE, Vagsholm I (2009) Causes of mortality in laying hens in different housing systems in 2001 to 2004. Acta Vet Scand 51:3

    PubMed  PubMed Central  Google Scholar 

  • Frölich S, Entzeroth R, Wallach M (2012) Comparison of protective immune responses to apicomplexan parasites. J Parasitol Res 2012:852591

    PubMed  PubMed Central  Google Scholar 

  • Frölich S, Johnson M, Robinson M, Entzeroth R, Wallach M (2013) The spatial organization and extraction of the wall-forming bodies of Eimeria maxima. Parasitology 140:876–887

    PubMed  Google Scholar 

  • Gabrashanska M, Kolnarski V, Anisimova M, Denev S (2009) Influence of selenium and Eimeria tenella infection on antioxidant status in chickens. Trace Elem Elec 26:17–23

    CAS  Google Scholar 

  • Georgieva NV, Gabrashanska M, Kolnarski V (2011a) Antioxidant status in Eimeria acervulina infected chickens after dietary selenium treatment. Trace Elem Elec 28:42–48

    CAS  Google Scholar 

  • Georgieva NV, Gabrashanska M, Kolnarski V, Yaneva Z (2011b) Zinc supplementation against Eimeria acervulina-induced oxidative damage in broiler chickens. Vet Med Intern 2011:647124

    Google Scholar 

  • Ghazanfari T, Hassan ZM, Khamesipour A (2006) Enhancement of peritoneal macrophage phagocytic activity against Leishmania major by garlic (Allium sativum) treatment. J Ethnopharmacol 103:333–337

    PubMed  Google Scholar 

  • Greif G, Harder A, Haberkorn A (2001) Chemotherapeutic approaches to protozoa: Coccidiae–current level of knowledge and outlook. Parasitol Res 87:973–975

    PubMed  CAS  Google Scholar 

  • Haberkorn A, Harder A, Greif G (2001) Milestones of protozoan research at Bayer. Parasitol Res 87:1060–1062

    PubMed  CAS  Google Scholar 

  • Hackstein JH, Mackenstedt U, Mehlhorn H, Meijerink JP, Schubert H, Leunissen JH (1995) Parasitic apicomplexans harbor a chlorophyll a-D1 complex, the potential target for therapeutic triazinones. Parasitol Res 81:207–216

    PubMed  CAS  Google Scholar 

  • Harder A, Haberkorn A (1989) Possible mode of action of toltrazuril: studies on two Eimeria species and mammalian and Ascaris suum enzymes. Parasitol Res 76:8–12

    PubMed  CAS  Google Scholar 

  • Hong SH, Lee HKK, Song J, Son MW, Kim O (2008) The effects of natural herbal antibacterial compound against enteropathogenic Escherichia coli. Lab Anim Res 24:341–346

    Google Scholar 

  • Hosse RJ, Krucken J, Bierbaum S, Greif G, Wunderlich F (2008) Eimeria tenella: genomic organization and expression of an 89 kDa cyclophilin. Exp Parasitol 118:275–279

    PubMed  CAS  Google Scholar 

  • Huang Z, Rose AH, Hoffmann PR (2012) The role of selenium in inflammation and immunity: from molecular mechanisms to therapeutic opportunities. Antioxid Redox Signal 16:705–743

    PubMed  PubMed Central  CAS  Google Scholar 

  • Hussein WM, Liu TY, Skwarczynski M, Toth I (2014) Toll-like receptor agonists: a patent review (2011–2013). Expert Opin Ther Pat 4:453–470

    Google Scholar 

  • Jafari RK, Shahriyari A, Assadi F, Hamidi-Nejat H (2012) Effect of dietary vitamin E on Eimeria tenella-induced oxidative stress in broiler chickens. Afr J Biotechnol 11:9265–9269

    CAS  Google Scholar 

  • Jones D, Sies H (2007) Oxidative stress. In: Fink G (ed) Encyclopedia of stress, vol 3. Academic, San Diego, pp 45–48

    Google Scholar 

  • Kar A, Choudhary BK, Bandyopadhyay NG (2003) Comparative evaluation of hypoglycaemic activity of some Indian medicinal plants in alloxan diabetic rats. J Ethnopharmacol 84:105–108

    PubMed  Google Scholar 

  • Karasaki Y, Tsukamoto S, Mizusaki K, Sugiura T, Gotoh S (2001) A garlic lectin exerted an antitumor activity and induced apoptosis in human tumor cells. Food Res Int 34:7–13

    CAS  Google Scholar 

  • Kawai T, Akira S (2011) Toll-like receptors and their crosstalk with other innate receptors in infection and immunity. Immunity 34:637–650

    PubMed  CAS  Google Scholar 

  • Khalafalla RE, Müller U, Shahiduzzaman M, Dyachenko V, Desouky AY, Alber G, Daugschies A (2011) Effects of cucurmin (diferuloylmezhane) on Eimeria tenella sporozoites in vitro. Parasitol Res 108:879–886

    PubMed  Google Scholar 

  • Korayem AM, Hasabo SA, Ameen HH (1993) Effects and mode of action of some plant extracts on certain plant parasitic nematodes. Anz Schadl 66:32–36

    Google Scholar 

  • Kumar S, Gupta AK, Pal Y, Dwivedi SK (2003a) In-vivo therapeutic efficacy trial with artemisinin derivative, buparvaquone and imidocarb dipropionate against Babesia equi infection in donkeys. J Vet Med Sci 65:1171–1177

    PubMed  CAS  Google Scholar 

  • Kumar VG, Surendranathan KP, Umesh KC, Devi DRG, Belwadi MR (2003b) Effect of onion (Allium cepa Linn.) and garlic (Allium sativum Linn.) on plasma triglyceride content in Japanese quail (Coturnix coturnix japonicum). Indian J Exp Biol 41:88–90

    PubMed  Google Scholar 

  • Lambert RJW, Skandamis PN, Coote PJ, Nychas GJE (2001) A study of the minimum inhibitory concentration and mode of action of oregano essentials oil, thymol and carvacrol. J Appl Microbiol 91:453–462

    PubMed  CAS  Google Scholar 

  • Lee HA, Hewang KK, Song JH, Kim O (2008a) The effects of an herbal antimicrobial feed additive on the health status and performance of growing and finishing pigs. Lab Anim Res 24:187–192

    Google Scholar 

  • Lee HA, Park H, Kim YC, Kim O (2008b) The effects of natural herbal antiviral compound against porcine epidemic diarrhea virus. Lab Anim Res 24:179–185

    Google Scholar 

  • Lee HA, Hong S, Chung Y-H, Song K-D, Kim O (2012) Anticoccidial effects of Galla rhois extract on Eimeria tenella-infected chicken. Lab Anim Res 28:193–197

    PubMed  PubMed Central  Google Scholar 

  • Lee SH, Lillehoj HS, Jang SI, Jeong MS, Xu SZ, Kim JB, Park HJ, Kim HR, Lillehoj EP, Bravo DM (2014) Effects of in ovo injection with selenium on immune and antioxidant responses during experimental necrotic enteritis in broiler chickens. Poult Sci 93:1113–1121

    PubMed  CAS  Google Scholar 

  • Maruyama T, Furutani M (2000) Archaeal peptidyl prolyl cis-trans isomerases (PPIases). Front Biosci 5:D821–D836

    PubMed  CAS  Google Scholar 

  • Masood S, Abbas RZ, Iqbal Z, Mansoor MK, Sindhu Z, Zia MA, Khan JA (2013) Role of natural antioxidants for the control of coccidiosis in poultry. Pak Vet J 33:401–407

    CAS  Google Scholar 

  • Mathis GF, Froyman R, Kenedy T (2004) Coccidiosis control by administering toltrazuril in the drinking water for a 2-day period. Vet Parasitol 121:1–9

    PubMed  CAS  Google Scholar 

  • Mehlhorn H (ed) (2014) Encyclopedic reference of parasitology, 4th edn. Springer, Berlin

    Google Scholar 

  • Mehlhorn H, Ortmann-Falkenstein G, Haberkorn A (1984) The effects of sym. triazinones on developmental stages of Eimeria tenella, E. maxima and E. acervulina: a light and electron microscopical study. Parasitol Res 70:173–182

    CAS  Google Scholar 

  • Metwaly MS, Dkhil MA, Al-Quraishy S (2012a) The potential role of Phoenix dactylifera on Eimeria papillata-induced infection in mice. Parasitol Res 111:681–687

    PubMed  Google Scholar 

  • Metwaly MS, Dkhil MA, Al-Quraishy S (2012b) Role of Phoenix dactylifera in ameliorating Eimeria papillata-induced hepatic injury in mice. J Med Plant Res 6:3041–3047

    Google Scholar 

  • Mishina YV, Krishna S, Haynes RK, Meade JC (2007) Artemisinins inhibit Trypanosoma cruzi and Trypanosoma brucei rhodesiense in vitro growth. Antimicrob Agents Chemother 51:1852–1854

    PubMed  PubMed Central  CAS  Google Scholar 

  • Mundt HC, Daugschies A, Uebe F, Rinke M (2003) Efficacy of toltrazuril against artificial infections with Eimeria bovis in calves. Parasitol Res 90:S166–S167

    PubMed  Google Scholar 

  • Mundt HC, Mundt-Wustenberg S, Dugschies A, Joachim A (2007) Efficacy of various anticoccidials against experimental porcine neonatal isosporosis. Parasitol Res 100:401–412

    PubMed  CAS  Google Scholar 

  • Mundt HC, Dittmar K, Daugschies A, Grzonka E, Bangoura B (2009) Study of the comparative efficacy of toltrazuril and diclazuril against ovine coccidiosis in housed lambs. Parasitol Res 105:S141–S150

    PubMed  Google Scholar 

  • Nathan C, Cunningham-Bussel A (2013) Beyond oxidative stress: an immunologist's guide to reactive oxygen species. Nat Rev Immunol 13:349–361

    PubMed  CAS  Google Scholar 

  • Nielsen FH (2012) History of zinc in agriculture. Adv Nutr 3:783–789

    PubMed  PubMed Central  CAS  Google Scholar 

  • Nok AJ, Williams S, Onyenekwe PC (1996) Allium sativum-induced death of African trypanosomes. Parasitol Res 82:634–637

    PubMed  CAS  Google Scholar 

  • Pakandl M (2005) Selection of precocious line of the rabbit coccidium Eimeria flavescens Marotel and Guilhon (1941) and characterisation of its endogenous cycle. Parasitol Res 97:150–155

    PubMed  CAS  Google Scholar 

  • Peyghan R, Powell MD, Zadkarami MR (2008) In vitro effect of garlic extract and metronidazole against Neoparamoeba pemaquidensis, page 1987, and isolated amoebae from Atlantic salmon. Pak J Biol Sci 11:41–47

    PubMed  CAS  Google Scholar 

  • Pradhan KD, Thakur DK, Sudhan NA (1992) Therapeutic efficacy of Punica granatum and Cucurbita maxima against clinical cases of nematodiasis in calves. Indian J Indigenous Med 9:53–55

    Google Scholar 

  • Prolo C, Alvarez MN, Radi R (2014) Peroxynitrite, a potent macrophage-derived oxidizing cytotoxin to combat invading pathogens. Biofactors 40:215–225

    PubMed  CAS  Google Scholar 

  • Puertollano MA, Puertollano E, de Cienfuegos GA, de Pablo MA (2011) Dietary antioxidants: immunity and host defense. Curr Top Med Chem 11:1752–1766

    PubMed  CAS  Google Scholar 

  • Raji Y, Ogunwande IA, Osadebe CA, John G (2004) Effects of Azadirachta indica extract on gastric ulceration and acid secretion in rats. J Ethnopharmacol 90:167–170

    PubMed  Google Scholar 

  • Rayman MP (2012) Selenium and human health. Lancet 379:1256–1268

    PubMed  CAS  Google Scholar 

  • Ryley JF, Robinson TE (1976) Life cycle studies with Eimeria magna (Perard, 1925). Parasitol Res 12:257–275

    Google Scholar 

  • Saafi EB, Louedi M, Elfeki A, Zakhama A, Najjar MF, Hammami M, Achour L (2011) Protective effect of date palm fruit extract (Phoenix dactylifera L.) on dimethoate inducedoxidative stress in rat liver. Exp Toxicol Pathol 63:433–441

    PubMed  CAS  Google Scholar 

  • Sarac N, Ugur A, Duru ME, Varol O (2009) Antimicrobial activity, antioxidant activity and chemical composition Origanum onites L. and Origanum vulgare L. ssp. hirtum (Link) ietswaart from Mugla (Turkey). Acta Horticult 826:397–404

    CAS  Google Scholar 

  • Savva A, Roger T (2013) Targeting Toll-like receptors: promising therapeutic strategies for the management of sepsis-associated pathology and infectious diseases. Front Immunol 4:1–16

    Google Scholar 

  • Schneider H, Charara N, Schmitz R, Wehrli S, Mikol V, Zurini MG, Quesniaux VF, Movva NR (1994) Human cyclophilin C: primary structure, tissue distribution, and determination of binding specificity for cyclosporins. Biochemistry 33:8218–8224

    PubMed  CAS  Google Scholar 

  • Seemann E, Kurth T, Entzeroth R (2012) Insight into the ultrastructural organisation of sporulated oocysts of Eimeria nieschulzi (Coccidia, Apicomplexa). Parasitol Res 111:2143–2147

    PubMed  Google Scholar 

  • Shirley MW, Smith AL, Tomley FM (2005) The biology of avian Eimeria with an emphasis on their control by vaccination. Adv Parasitol 60:285–330

    PubMed  Google Scholar 

  • Sies H (1986) Biochemistry of oxidative stress. Angew Chem Int Ed 25:1058–1071

    Google Scholar 

  • Sies H (1993) Strategies of antioxidant defense. Eur J Biochem 215:213–219

    PubMed  CAS  Google Scholar 

  • Sies H (2014) Role of metabolic H2O2 generation: redox signaling and oxidative stress. J Biol Chem 289:8735–8741

    PubMed  CAS  Google Scholar 

  • Spallholz JE, Hoffmann DJ (2002) Selenium toxicity: cause and effects in aquatic birds. Aquatic Toxicol 57:27–37

    CAS  Google Scholar 

  • Speckmann B, Steinbrenner H (2014) Selenium and selenoproteins in inflammatory bowel diseases and experimental colitis. Inflamm Bowel Dis 20:1110–1190

    PubMed  Google Scholar 

  • Speckmann B, Bidmon H-J, Borchardt A, Sies H, Steinbrenner H (2014) Intestinal selenoprotein P in epithelial cells and in plasma cells. Arch Biochem Biophys 541:30–36

    PubMed  CAS  Google Scholar 

  • Steinbrenner H, Sies H (2009) Protection against reactive oxygen species by selenoproteins. Biochim Biophys Acta 1790:1478–1485

    PubMed  CAS  Google Scholar 

  • Sundaram SG, Milner JA (1996) Diallyl disulfide inhibits the proliferation of human tumor cells in culture. Biochim Biophys Acta 1315:15–20

    PubMed  Google Scholar 

  • Szaboova R, Laukova A, Chrstinova L, Strompfova V, Simonova PM, Placha I, Vasilkova Z, Chrenkova M, Faix S (2012) Beneficial effect of plant extracts in rabbit husbandry. Acta Vet BRNO 81:245–259

    CAS  Google Scholar 

  • Traber MG, Sies H (1996) Vitamin E in humans: demand and delivery. Annu Rev Nutr 16:321–347

    PubMed  CAS  Google Scholar 

  • Turk DE, Stephens JF (1966) Effect of intestinal damage produced by Eimeria necatrix infection in chicks upon absorption of orally administered zinc-65. J Nutr 88:261–266

    PubMed  CAS  Google Scholar 

  • Vuddanda PR, Chakraborty S, Siungh S (2010) Berberine: a potential phytochemical with multispectrum therapeutic activities. Expert Opin Invest Druds 19:1297–1307

    CAS  Google Scholar 

  • Wahba A (2003) Studies on the efficacy of garlic extract on cryptosporidiosis in experimentally infected mice. J Egypt Soc Parasitol 81:793–803

    Google Scholar 

  • Wallach M, Smith NC, Petracca M, Miller CMD, Eckert J, Braun R (1992) Eimeria maxima gametocyte antigens: potential use in a subunit maternal vaccine against coccidiosis in chickens. Vaccine 13:347–354

    Google Scholar 

  • Wallach MG, Ashash U, Michael A, Smith NC (2008) Field application of a subunit vaccine against an enteric protozoan disease. PLoS One 3:e3948

    PubMed  PubMed Central  Google Scholar 

  • Wang P, Heitmann J (2005) The cyclophilins. Genome Biol 6:226

    PubMed  PubMed Central  Google Scholar 

  • Weathers PJ, Jordan NJ, Lasin P, Towler MJ (2014) Simulated digestion of dried leaves of Artemisia annua consumed as a treatment (pACT) for malaria. J Ethnopharmacol 151:858–863

    PubMed  Google Scholar 

  • Williams R (1999) A compartmentalised model for the estimation of the cost of coccidiosis to the world's chicken production industry. Intern J Parasitol 29:285–330

    Google Scholar 

  • Williams R (2002) Anticoccidial vaccines for broiler chickens: pathways to success. Avian Pathol 31:317–353

    PubMed  CAS  Google Scholar 

  • Wongbutde E (2008) Physiological effects of berberine. Thai Pharm Hlth Sci J 4:78–83

    Google Scholar 

  • Wunderlich CM, Delić D, Behnke K, Meryk A, Ströhle P, Chaurasia B, Al-Quraishy S, Wunderlich F, Brüning JC, Wunderlich FT (2012) Inhibition of IL-6 trans-signaling protects from malaria-induced lethality in mice. J Immunol 188:4141–4144

    PubMed  CAS  Google Scholar 

  • Yang DM, Liew FY (1993) Effects of qinghaosu (artemisinin) and its derivatives on experimental cutaneous leishmaniasis. Parasitology 106:7–11

    PubMed  CAS  Google Scholar 

  • Yao Q, Li M, Yang H, Chai H, Fischer W, Chen C (2005) Roles of cyclophilins in cancers and other organ systems. World J Surg 29:276–280

    PubMed  Google Scholar 

  • Yoshida H, Iwata N, Katzusaki H, Naganawa R, Ishikawa R, Fukuda H, Fijinu T, Suzuki A (1998) Antimicrobial activity of a compound isolated from an oil-macerated garlic extract. Biosci Biotechnol Biochem 62:1014–1017

    PubMed  CAS  Google Scholar 

  • Zhang L, Liu R, Song M, Hu Y, Pan B, Cai J, Wang M (2013) Eimeria tenella: interleukin 17 contributes to host immunopathology in the gut during experimental infection. Exp Parasitol 133:121–130

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

The authors appreciate the Distinguished Scientist Fellowship Program, King Saud University, Saudi Arabia.

Author information

Authors and Affiliations

  1. Department of Biology, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany

    Frank Wunderlich

  2. Department of Zoology, College of Science, King Saud University, P.O. Box 2455, Riyadh, 11451, Saudi Arabia

    Saleh Al-Quraishy, Helmut Sies & Mohamed A. Dkhil

  3. Institute of Biochemistry and Molecular Biology I, Heinrich-Heine-University Düsseldorf, Düsseldorf, Germany

    Holger Steinbrenner & Helmut Sies

  4. Department of Zoology and Entomology, Faculty of Science, Helwan University, Helwan, Egypt

    Mohamed A. Dkhil

Authors
  1. Frank Wunderlich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Saleh Al-Quraishy
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Holger Steinbrenner
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Helmut Sies
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Mohamed A. Dkhil
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Mohamed A. Dkhil.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wunderlich, F., Al-Quraishy, S., Steinbrenner, H. et al. Towards identifying novel anti-Eimeria agents: trace elements, vitamins, and plant-based natural products. Parasitol Res 113, 3547–3556 (2014). https://doi.org/10.1007/s00436-014-4101-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00436-014-4101-8

Keywords

Search

Navigation