Advertisement

Natural Products as Antiparasitic Agents

  • Lucie Paloque
  • Asih Triastuti
  • Geneviève Bourdy
  • Mohamed Haddad
Chapter
Part of the Sustainable Development and Biodiversity book series (SDEB, volume 19)

Abstract

Parasitic diseases remain a major burden on global human and veterinary health. They affect more than two billion people worldwide causing considerable morbidity and mortality and are a major constraint on livestock production, especially in the world’s poorest communities. The immense suffering caused by these illnesses and the consequential loss of productivity is a major drain on the limited resources of the populations in which they occur. Most modern and effective drugs for parasitic diseases present no financial viability for the pharmaceutical industry since affected people have limited financial resources. Although financial return on investment is insufficient for drug discovery process and development, there is a constant desperate need for new chemical entities presenting new mechanisms of action. Higher plants, marine organisms, and microorganisms provide immense opportunities for the discovery of new drugs and drug leads. The screening of these natural sources thus remains one of the most attractive routes to discovering and developing new drugs. This article reviews the importance of natural products as a source of antiparasitic drugs and discusses some of the research challenges.

Keywords

Natural products Antimicrobial Human/animal parasitic disease Drug discovery 

References

  1. Abbas R, Colwell D, Gilleard J (2012) Botanicals: an alternative approach for the control of avian coccidiosis. Worlds Poult Sci J 68(2):203–215Google Scholar
  2. Atanasov AG, Waltenberger B, Pferschy-Wenzig EM, Linder T, Wawrosch C, Uhrin P, Temml V, Wang L, Schwaiger S, Heiss EH, Rollinger JM, Schuster D, Breuss JM, Bochkov V, Mihovilovic MD, Kopp B, Bauer R, Dirsch VM, Stuppner H (2015) Discovery and resupply of pharmacologically active plant-derived natural products: A review. Biotechnol Adv 33(8):1582–1614CrossRefPubMedPubMedCentralGoogle Scholar
  3. Aubertin C, Filoche G (2011) The Nagoya protocol on the use of genetic resources: one embodient of an endless discussion. Sustenabilidade em Debate 2(1):51–64Google Scholar
  4. Bessoff K, Spangenberg T, Foderaro JE, Jumani RS, Ward GE, Hustona CD (2014) Identification of Cryptosporidium parvum active chemical series by Repurposing the open access malaria box. Antimicrob Agents Chemother 58(5):2731–2739Google Scholar
  5. Blake DP, Tomley FM (2014) Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol 30(1):12–19CrossRefPubMedGoogle Scholar
  6. Blunt JW, Copp BR, Keyzers RA, Munro MH, Prinsep MR (2016) Marine natural products. Nat Prod Rep 33(3):382–431Google Scholar
  7. Braga ÉM, Silveira P, Belo NO, Valkiũnas G (2011) Recent advances in the study of avian malaria: an overview with an emphasis on the distribution of Plasmodium spp in Brazil. Mem Inst Oswaldo Cruz 106:3–11Google Scholar
  8. Bucar F, Wube A, Schmid M (2013) Natural product isolation - how to get from biological material to pure compounds. Nat Prod Rep 30:525–545CrossRefPubMedGoogle Scholar
  9. Butler MS, Robertson AAB, Cooper MA (2014) Natural product and natural product derived drugs in clinical trials. Nat Prod Rep 31:1612–1661CrossRefPubMedGoogle Scholar
  10. Cardona GA, Carmena D (2013) A review of the global prevalence, molecular epidemiology and economics of cystic echinococcosis in production animals. Vet Parasitol 192(1–3):10–32CrossRefPubMedGoogle Scholar
  11. Chapman HD (2014) Milestones in avian coccidiosis research: a review. Poult Sci 93:501–511CrossRefPubMedGoogle Scholar
  12. Charlier J, van der Voort M, Kenyon F, Skuce P, Vercruysse J (2014) Chasing helminths and their economic impact on farmed ruminants. Trends Parasitol 30(7):361–367CrossRefPubMedGoogle Scholar
  13. Checkley W, White AC Jr, Jaganath D, Arrowood MJ, Chalmers RM, Chen XM, Fayer R, Griffiths JK, Guerrant RL, Hedstrom L, Huston CD, Kotloff KL, Kang G, Mead JR, Miller M, Petri WA Jr, Priest JW, Roos DS, Striepen B, Thompson RC, Ward HD, Van Voorhis WA, Xiao L, Zhu G, Houpt ER (2015) A review of the global burden, novel diagnostics, therapeutics, and vaccine targets for cryptosporidium. Lancet Infect Dis 15(1):85–94Google Scholar
  14. Colley DG (2000) Parasitic diseases: opportunities and challenges in the 21st century. Mem Inst Oswaldo Cruz 95:79–87Google Scholar
  15. Cordell GA, Colvard MD (2012) Natural products and traditional medicine: turning on a paradigm. J Nat Prod 75(3):514–525Google Scholar
  16. Cragg GM, Newman DJ, Snader KM (1997) Natural products in drug discovery and development. J Nat Prod 60(1):52–60CrossRefPubMedGoogle Scholar
  17. Crosia PJ (2011) Worldwide market of veterinary drugs: trend analysis for the last ten years. Bull Acad Vet France 164(1):21–25CrossRefGoogle Scholar
  18. David B, Wolfender JL, Dias DA (2015) The pharmaceutical industry and natural products: historical status and new trends. Phytochem Rev 14(2):299–315CrossRefGoogle Scholar
  19. DeFelice SL (2002) FIM rationale and proposed guidelines for the nutraceutical research & education Act - NREA, November 10, 2002. Foundation for Innovation in Medicine. http://www.fimdefelice.org/archives/arc.researchact.html
  20. De Souza W, Rodrigues JCF (2009) Sterol biosynthesis pathway as target for anti-trypanosomatid drugs. Interdiscip Perspect Infect Dis.  https://doi.org/10.1155/2009/642502PubMedPubMedCentralGoogle Scholar
  21. EMEA (1998) Quality of herbal medicinal products. Guidelines, European Agency for the Evaluation of Medicinal Products (EMEA), LondonGoogle Scholar
  22. Epe C, Kaminsky R (2013) New advancement in anthelmintic drugs in veterinary medicine. Trends Parasitol 29(3):129–134CrossRefPubMedGoogle Scholar
  23. Fernańdez-Álvaro E, Hong WD, Nixon GL, O’Neill PM, Calderoń F (2016) Antimalarial chemotherapy: natural product inspired development of preclinical and clinical candidates with diverse mechanisms of action. J Med Chem 59:5587–5603CrossRefPubMedGoogle Scholar
  24. Geary TG, Woo K, McCarthy JS, Mackenzie CD, Horton J, Prichard RK, de Silva NR, Olliaro PL, Lazdins-Helds JK, Engels DA, Bundy DA (2010) Unresolved issues in anthelmintic pharmacology for helminthiases of humans. Int J Parasitol 40(1):1–13CrossRefPubMedGoogle Scholar
  25. Geerts S, Holmes PH, Diall O, Eisler MC (2001) African bovine trypanosomiasis: the problem of drug resistance. Trends Parasitol 17(1):25–28Google Scholar
  26. Geurden T, Chartier C, Fanke J, Frangipane di Regalbone A, Travaersa D, von Samason-Himmelstjerna G, Demeler J, Vanimisetti HB, Bartam DJ, Denwood MJ (2015) Anthelmintic resistance to ivermectin and moxidectin in gastrointestinal nematodes of cattle in Europe. Int J Parasitol Drugs Drug Resist 5(3):163–171CrossRefPubMedPubMedCentralGoogle Scholar
  27. Gohil S, Herrmann S, Günther S, Cooke BM (2013) Bovine babesiosis in the 21st century: advances in biology and functional genomics. Int J Parasitol 43(2):125–132CrossRefPubMedGoogle Scholar
  28. Goldman Sachs (2015) Mectizan donation program, Annual highlights. http://www.goldmansachs.com/media-relations/press-releases/current/pdfs/2013-q4-results.pdf
  29. Goo YK, Terkawi MA, Jia H, Aboge GO, Ooka H, Nelson B, Kim S, Sunaga F, Namikawa K, Igarashi I, Nishikawa Y, Xuan X (2010) Artesunate, a potential drug for treatment of Babesia infection. Parasitol Int 59(3):481–486CrossRefPubMedGoogle Scholar
  30. Hertweck C (2015) Natural products as source of therapeutics against parasitic diseases. Angew Chem Int Ed Engl 54(49):14622–14624CrossRefPubMedGoogle Scholar
  31. Horn D, Duraisingh MT (2014) Antiparasitic chemotherapy: from genomes to mechanisms. Annu Rev Pharmacol Toxicol 54:71–94Google Scholar
  32. Hoste H, Torres-Acosta JFJ, Sandoval-Castro CA, Mueller-Harvey I, Sotiraki S, Louvandini H, Thamsborg SM, Terrill TH (2015) Tannin containing legumes as a model for nutraceuticals against digestive parasites in livestock. Vet Parasitol 15;212(1–2):5–17Google Scholar
  33. Hotez PJ, Alvarado M, Basanez MG, Bolliger I, Bourne R, Boussinesq M, Brooker SJ, Brown AS, Buckle G, Budke CM, Carabin H, Coffeng LE, Fèvre EM, Fürst T, Halasa YA, Jasrasaria R, Johns NE, Keiser J, King CH, Lozano R, Murdoch ME, O’Hanlon S, Pion SD, Pullan RL, Ramaiah KD, Roberts T, Shepard DS, Smith JL, Stolk WA, Undurraga EA, Utzinger J, Wang M, Murray CJ, Naghavi M (2014) The global burden of disease study 2010: interpretation and implications for the neglected tropical diseases. PLoS Negl Trop Dis 8(7):e2865Google Scholar
  34. Hussain H, Al-Harrasi A, Al-Rawahi A, Green IR, Gibbons S (2014) Fruitful decade for antileishmanial compounds from 2002 to late 2011. Chem Rev 114(20):10369–10428Google Scholar
  35. Iguchi A, Matsuu A, Matsuyama K, Hikasa Y (2015) The efficacy of artemisinin, artemether, and lumefantrine against Babesia gibsoni in vitro. Parasitol Int 64(2):190–193CrossRefPubMedGoogle Scholar
  36. Jones WP, Kinghorn AD (2012) Extraction of plant secondary metabolites. Methods Mol Biol 864:341–366CrossRefPubMedGoogle Scholar
  37. Kalra EK (2003) Nutraceutical: definition and introduction. AAPS pharmSci 5(3):E25Google Scholar
  38. Kayser O, Kiderlen AF, Croft SL (2003) Natural products as antiparasitic drugs. Parasitol Res 90:S55–S62CrossRefPubMedGoogle Scholar
  39. Kessl JJ, Meshnick SR, Trumpower BL (2007) Modeling the molecular basis of atovaquone resistance in parasites and pathogenic fungi. Trends Parasitol 23(10):494–501CrossRefPubMedGoogle Scholar
  40. Khan MK, Sajid MS, Riaz H, Ahmad NE, He L, Shahzad M, Hussain A, Khan MN, Iqbal Z, Zhao J (2013) The global burden of fasciolosis in domestic animals with an outlook on the contribution of new approaches for diagnosis and control. Parasitol Res 112(7):2421–2430Google Scholar
  41. Kim DK, Lillehoj HS, Lee SH, Jang SI, Lillehoj EP, Bravo D (2013) Dietary Curcuma longa enhances resistance against Eimeria maxima and Eimeria tenella infections in chickens. Poult Sci 92(10):2635–2643CrossRefPubMedGoogle Scholar
  42. Knubben-Schweizer G, Torgerson PR (2015) Bovine fasciolosis: control strategies based on the location of Galba truncatula habitats on farms. Vet Parasitol 208(1–2):77–83Google Scholar
  43. Königová A, Várady M, Čorba J (2003) Comparison of in vitro methods and faecal egg count reduction test for the detection of benzimidazole resistance in small strongyles of horses. Vet Res Commun 27(4):281–288CrossRefPubMedGoogle Scholar
  44. Krauth-Siegel RL, Comini MA (2008) Redox control in trypanosomatids, parasitic protozoa with trypanothione-based thiol metabolism. Biochim Biophys Acta 1780(11):1236–1248Google Scholar
  45. Kumar S, Gupta AK, Pal Y, Dwivedi SK (2003) In-vivo therapeutic efficacy trial with artemisinin derivative, buparvaquone and imidocarb dipropionate against Babesia equi infection in donkeys. J Vet Med Sci 65(11):1171–1177CrossRefPubMedGoogle Scholar
  46. Lanusse C, Alvarez L, Lifschitz A (2014) Pharmacological knowledge and sustainable anthelmintic therapy in ruminants. Vet Parasitol 204(1–2):18–33CrossRefPubMedGoogle Scholar
  47. Lathers CM (2003) Challenges and opportunities in animal drug development: a regulatory perspective. Nat Rev Drug Discov 2(11):915–918CrossRefPubMedGoogle Scholar
  48. Mazuz ML, Golenser J, Fish L, Haynes RK, Wollkomirsky R, Leibovich B, Shkap V (2013) Artemisone inhibits in vitro and in vivo propagation of Babesia bovis and B. bigemina parasites. Exp Parasitol 135(4):690–694CrossRefPubMedGoogle Scholar
  49. McKerrow JH (2015) Recognition of the role of Natural Products as drugs to treat neglected tropical diseases by the 2015 Nobel prize in physiology or medicine. Nat Prod Rep 32:1610–1611CrossRefPubMedGoogle Scholar
  50. Molan AL, Liu Z, De S (2009) Effect of pine bark (Pinus radiata) extracts on sporulation of coccidian oocysts. Folia Parasitol (Praha). 56(1):1–5CrossRefPubMedGoogle Scholar
  51. Morrison WI (2015) The aetiology, pathogenesis and control of theileriosis in domestic animals. Rev Sci Tech 34(2):599–611Google Scholar
  52. Mosqueda J, Olvera-Ramirez A, Aguilar-Tipacamu G, Canto GJ (2012) Current advances in detection and treatment of babesiosis. Curr Med Chem 19(10):1504–1518CrossRefPubMedPubMedCentralGoogle Scholar
  53. Müller J, Hemphill A (2013) New approaches for the identification of drug targets in protozoan parasites. Int Rev Cell Mol Biol 301:359–401Google Scholar
  54. Müller J, Hemphill A (2016) Drug target identification in protozoan parasites. Expert Opin Drug Discov 11(8):815–824Google Scholar
  55. Muthamilselvan T, Kuo TF, Wu YC, Yang WC (2016) Herbal remedies for coccidiosis control: a review of plants, compounds, and anticoccidial actions. Evid Based Complement Alternat Med:1–19Google Scholar
  56. Ndjonka D, Rapado LN, Silber AM, Liebau E, Wrenger C (2013) Natural products as a source for treating neglected parasitic diseases. Int J Mol Sci 14(2):3395–3439Google Scholar
  57. Newman DJ, Cragg GM (2012) Natural products as sources of new drugs over the 30 years from 1981 to 2010. J Nat Prod 75(3):311–335Google Scholar
  58. Newman DJ, Cragg GM (2016) Natural products as sources of new drugs from 1981 to 2014. J Nat Prod 79(3):629–661CrossRefPubMedGoogle Scholar
  59. Ngo LT, Okogun JI, Folk WR (2013) 21st century natural product research and drug development and traditional medicines. Nat Prod Rep 30(4):584–592Google Scholar
  60. Nosengo N (2016) Can you teach old drugs new tricks? Nature 14;534(7607):314–316Google Scholar
  61. Olliaro P, Seiler J, Kuesel A, Horton J, Clark JN, Don R, Keiser J (2011) Potential drug development candidates for human soil-transmitted helminthiases. PLoS Negl Trop Dis 5(6):e1138Google Scholar
  62. Paloque L, Ramadani AP, Mercereau–Puijalon O, Augereau JM, Benoit–Vical F (2016) Plasmodium falciparum: multifaceted resistance to artemisinins. Malar J 15:149Google Scholar
  63. Patz JA, Graczyk TK, Geller N, Vittor AY (2000) Effects of environmental change on emerging parasitic diseases. Int J Parasitol 30(12–13):1395–1405Google Scholar
  64. Patwardhan B (2005) Ethnopharmacology and drug discovery. J Ethnopharmacol 100(1–2):50–52CrossRefPubMedGoogle Scholar
  65. Pink R, Hudson A, Mouriès MA, Bendig M (2005) Opportunities and challenges in antiparasitic drug discovery. Nat Rev Drug Discov 4(9):727–740Google Scholar
  66. Quiroz-Castaneda RE, Dantan-Gonzalez E (2015) Control of avian coccidiosis: future and present natural alternatives. Biomed Res Int.  https://doi.org/10.1155/2015/430610Google Scholar
  67. Rajput N, Ali S, Naeem M, Khan MA, Wang T (2014) The effect of dietary supplementation with the natural carotenoids curcumin and lutein on pigmentation, oxidative stability and quality of meat from broiler chickens affected by coccidiosis challenge. Br Poult Sci 55(4):501–509CrossRefPubMedGoogle Scholar
  68. Rana AK, Misra-Bhattacharya S (2013) Current drug targets for helminthic diseases. Parasitol Res 112:1819–1831CrossRefPubMedGoogle Scholar
  69. Roeber F, Jex AR, Gasser RB (2013) Impact of gastrointestinal parasitic nematodes of sheep, and the role of advanced molecular tools for exploring epidemiology and drug resistance—an Australian perspective. Parasit Vectors 6:153Google Scholar
  70. Saifi MA, Beg T, Harrath AH, Altayalan FSH, Quraishy SA (2013) Antimalarial drugs: mode of action and status of resistance. Afr J Pharm Pharmacol 7(5):148–156Google Scholar
  71. Shahiduzzaman M, Daugschies A (2012) Therapy and prevention of cryptosporidiosis in animals. Vet Parasitol 188(3–4):203–214Google Scholar
  72. Shears MJ, Botté CY, McFadden GI (2015) Fatty acid metabolism in the Plasmodium apicoplast: drugs, doubts and knockouts. Mol Biochem Parasitol 199(1–2):34–50Google Scholar
  73. Singh S, Pathak AK, Sharma RK, Khan M (2015) Effect of tanniferous leaf meal based multi-nutrient blocks on feed intake, hematological profile, immune response, and body weight changes in Haemonchus contortus infected goats. Vet World 8(5):572–579CrossRefPubMedPubMedCentralGoogle Scholar
  74. Skinner-Adams TS, Sumanadasa SD, Fisher GM, Davis RA, Doolan DL, Andrews KT (2016) Defining the target of antiparasitic compounds. Drug Discov Today 21(5):725–739Google Scholar
  75. Torgerson PR (2013) One world health: socioeconomic burden and parasitic disease control priorities. Vet Parasitol 195(3–4):223–232Google Scholar
  76. United Nations Population Fund (2012) Population dynamics in the least developed countries: challenges and opportunities for development and poverty reduction. http://www.unfpa.org/sites/default/files/pub-pdf/CP51265.pdf
  77. Vernerova E, Vondrova R, Kisova H, Svobodova V, Hera A (2009) Detection of benzimidazole resistance in gastrointestinal nematode parasites of sheep in the Czech Republic. Veterinari Medicina 54(10):467–472CrossRefGoogle Scholar
  78. Waller PJ (2006) From discovery to development: current industry perspectives for the development of novel methods of helminth control in livestock. Vet Parasitol 139(1–3):1–14Google Scholar
  79. Wink (2010) Occurrence and function of natural products in plants, in Phytochemistry and Pharmacognosy, [Eds.John M.Pezzuto, Massuo Jorge Kato], in Encyclopedia of Life Support Systems(EOLSS), Developed under the Auspices of the UNESCO, Eolss Publishers, Oxford, UKGoogle Scholar
  80. Wink M (2015) Modes of action of herbal medicines and plant secondary metabolites. Medicines 2(3):251–286Google Scholar
  81. Williams AR, Fryganas C, Ramsay A, Mueller-Harvey I, Thamsborg SM (2014a) Direct anthelmintic effects of condensed tannins from diverse plant sources against Ascaris suum. PLoS ONE 9(6):e97053Google Scholar
  82. Williams AR, Ropiak HM, Fryganas C, Desrues O, Mueller-Harvey I, Thamsborg SM (2014b) Assessment of the anthelmintic activity of medicinal plant extracts and purified condensed tannins against free-living and parasitic stages of Oesophagostomum dentatum. Parasit Vectors 7:518Google Scholar
  83. Woolhouse MEJ, Gowtage-Sequeria S (2005) Host range and emerging and reemerging pathogens. Emerg Infect Dis 11(12):1842–1847Google Scholar
  84. Zhou S, Koh HL, Gao Y, Gong ZY, Lee EJ (2004) Herbal bioactivation: the good, the bad and the ugly. Life Sci 74(8):935–968Google Scholar
  85. Ziegler S, Pries V, Hedberg C, Waldmann H (2013) Target identification for small bioactive molecules: finding the needle in the haystack. Angew Chem Int Ed Engl 52(10):2744–2792Google Scholar

Copyright information

© Springer International Publishing AG 2018

Authors and Affiliations

  • Lucie Paloque
    • 1
  • Asih Triastuti
    • 2
  • Geneviève Bourdy
    • 2
  • Mohamed Haddad
    • 2
  1. 1.UPR8241 CNRS Laboratoire de Chimie de Coordination, University of Toulouse 3ToulouseFrance
  2. 2.UMR 152, IRD-UPS Pharma-DEV, University of Toulouse 3ToulouseFrance

Personalised recommendations