Hostname: page-component-8448b6f56d-tj2md Total loading time: 0 Render date: 2024-04-25T01:20:27.073Z Has data issue: false hasContentIssue false
  • English
  • Français

In vitro screening of 51 birdsfoot trefoil (Lotus corniculatus L.; Fabaceae) strains for anti-parasitic effects against Haemonchus contortus

Published online by Cambridge University Press:  14 January 2019

Carly D. Barone Open the ORCID record for Carly D. Barone [Opens in a new window] ,
Anne M. Zajac ,
Sarah M. Ferguson ,
Rebecca N. Brown ,
Jess D. Reed ,
Christian G. Krueger  and
Katherine H. Petersson
Carly D. Barone*
Affiliation:
Department of Fisheries, Animal, and Veterinary Sciences, University of Rhode Island, 120 Flagg Road, CBLS Rm 177, Kingston, RI 02881, USA
Anne M. Zajac
Affiliation:
Biomedical Sciences and Pathobiology, VA-MD Regional College of Veterinary Medicine, Virginia Tech, Center for Molecular Medicine and Infectious Diseases, 1410 Prices Fork Road, Blacksburg, VA 24061, USA
Sarah M. Ferguson
Affiliation:
Department of Plant Sciences and Entomology, University of Rhode Island, 9 E Alumni Ave, Woodward Hall Rm 236, Kingston, RI 02881,USA
Rebecca N. Brown
Affiliation:
Department of Plant Sciences and Entomology, University of Rhode Island, 9 E Alumni Ave, Woodward Hall Rm 236, Kingston, RI 02881,USA
Jess D. Reed
Affiliation:
Animal Science, University of Wisconsin, Madison, 1675 Observatory Drive, Rm 1146, Madison, WI 53706, USA
Christian G. Krueger
Affiliation:
Animal Science, University of Wisconsin, Madison, 1675 Observatory Drive, Rm 1146, Madison, WI 53706, USA
Katherine H. Petersson
Affiliation:
Department of Fisheries, Animal, and Veterinary Sciences, University of Rhode Island, 120 Flagg Road, CBLS Rm 177, Kingston, RI 02881, USA
*
Author for correspondence: Carly D. Barone, E-mail: carly_barone@my.uri.edu
Get access Rights & Permissions [Opens in a new window]

Abstract

Secondary plant compounds have shown bioactivity against multi-drug resistant Haemonchus contortus in small ruminants. This study screened 51 strains of birdsfoot trefoil (BFT, Lotus corniculatus) crude aqueous extracts (BFT-AqE) for anti-parasitic activity in vitro against egg hatching, and of those 51 strains, 13 were selected for further testing of motility of first (L1) and third stage (L3) larvae, and exsheathment of L3. Proanthocyanidin content ranged between 1.4 and 63.8 mg PAC g−1 powder across the 51 BFT strains. When tested against egg hatching, 21 of the 51 aqueous extracts had an EC50 of 1–2 mg powder mL−1, 70% of the strains were >90% efficacious at 6 mg powder mL−1 and 11 of the strains were 100% efficacious at 3 mg powder mL−1 BFT-AqE. Across the 13 strains tested against L3, efficacy ranged from 0 to 75% exsheathment inhibition, and 17 to 92% L3 motility inhibition at a concentration of 25 mg powder mL−1 BFT-AqE. There was no correlation between the PAC content of BFT powders and the anti-parasitic activity of aqueous extracts, therefore other secondary compounds may have contributed to the observed anti-parasitic effects. Further testing of BFT using bioactivity-driven fractionation and screening of BFT populations for the identified anti-parasitic compounds is needed.

Keywords

Birdsfoot trefoilegg hatchlarval exsheathmentlarval motility
Type
Research Article
Information
Parasitology , Volume 146 , Issue 6 , May 2019 , pp. 828 - 836
Check for updates
Copyright
Copyright © Cambridge University Press 2019 

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Acharya, J, Hildreth, MB and Reese, RN (2014) In vitro screening of forty medicinal plant extracts from the United States Northern Great Plains for anthelmintic activity against Haemonchus contortus. Veterinary Parasitology 201, 75–81.Google Scholar
Adamu, M, Oshadu, OD and Ogbaje, CI (2010) Anthelminthic efficacy of aqueous extract of Acanthus montanus leaf against strongylid nematodes of small ruminants. African Journal of Traditional, Complementary, and Alternative Medicines: AJTCAM/African Networks on Ethnomedicines 7, 279–285.Google Scholar
Alonso-Diaz, MA, Torres-Acosta, JF, Sandoval-Castro, CA, Aguilar-Caballero, AJ and Hoste, H (2008) In vitro larval migration and kinetics of exsheathment of Haemonchus contortus larvae exposed to four tropical tanniniferous plant extracts. Veterinary Parasitology 153, 313–319.Google Scholar
Assis, LM, Bevilaqua, CML, Morais, SM, Vieira, LS, Costa, CTC and Souza, JAL (2003) Ovicidal and larvicidal activity in vitro of Spigelia anthelmia Linn. extracts on Haemonchus contortus. Veterinary Parasitology 117, 43–49.Google Scholar
Barone, CD, Zajac, AM, Manzi-Smith, LA, Howell, AB, Reed, JD, Krueger, CG and Petersson, KH (2018) Anthelmintic efficacy of cranberry vine extracts on ovine Haemonchus contortus. Veterinary Parasitology 253, 122–129.Google Scholar
Barrau, E, Fabre, N, Fouraste, I and 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, 531–538.Google Scholar
Bernes, G, Waller, PJ and Christensson, D (2000) The effect of birdsfoot trefoil (Lotus corniculatus) and white clover (Trifolium repens) in mixed pasture swards on incoming and established nematode infections in young lambs. Acta Veterinaria Scandinavica 41, 351–361.Google Scholar
Brunet, S and Hoste, H (2006) Monomers of condensed tannins affect the larval exsheathment of parasitic nematodes of ruminants. Journal of Agricultural and Food Chemistry 54, 7481–7487.Google Scholar
Brunet, S, Aufrere, J, El Babili, F, Fouraste, I and Hoste, H (2007) The kinetics of exsheathment of infective nematode larvae is disturbed in the presence of a tannin-rich plant extract (sainfoin) both in vitro and in vivo. Parasitology 134, 1253–1262.Google Scholar
Brunet, S, Jackson, F and Hoste, H (2008) Effects of sainfoin (Onobrychis viciifolia) extract and monomers of condensed tannins on the association of abomasal nematode larvae with fundic explants. International Journal for Parasitology 38, 783–790.Google Scholar
Conder, GA and Johnson, SS (1996) Viability of infective larvae of Haemonchus contortus, Ostertagia ostertagi, and Trichostrongylus colubriformis following exsheathment by various techniques. The Journal of Parasitology 82, 100–102.Google Scholar
Desrues, O, Fryganas, C, Ropiak, HM, Mueller-Harvey, I, Enemark, HL and Thamsborg, SM (2016) Impact of chemical structure of flavanol monomers and condensed tannins on in vitro anthelmintic activity against bovine nematodes. Parasitology 143, 444–454.Google Scholar
Feliciano, RP, Shea, MP, Shanmuganayagam, D, Krueger, CG, Howell, AB and Reed, JD (2012) Comparison of isolated cranberry (Vaccinium macrocarpon Ait.) proanthocyanidins to catechin and procyanidins A2 and B2 for use as standards in the 4-(dimethylamino) cinnamaldehyde assay. Journal of Agricultural and Food Chemistry 60, 4578–4585.Google Scholar
Ferreira, LE, Castro, PM, Chagas, AC, Franca, SC and Beleboni, RO (2013) In vitro anthelmintic activity of aqueous leaf extract of Annona muricata L. (Annonaceae) against Haemonchus contortus from sheep. Experimental Parasitology 134, 327–332.Google Scholar
Foo, LY, Newman, R, Waghorn, GC and McNabb, WC (1996) Proanthocyanidins from Lotus corniculatus. Phytochemistry 41, 617–621.Google Scholar
Grabber, J, Riday, H, Cassida, K, Griggs, T, Min, D and MacAdam, J (2014) Yield, morphological characteristics, and chemical composition of European-and Mediterranean-derived birdsfoot trefoil cultivars grown in the colder continental United States. Crop Science 54, 1893–1901.Google Scholar
Häring, DA, Suter, D, Amrhein, N and Luscher, A (2007) Biomass allocation is an important determinant of the tannin concentration in growing plants. Annals of Botany 99, 111–120.Google Scholar
Heckendorn, F, Häring, DA, Maurer, V, Senn, M and Hertzberg, H (2007) Individual administration of three tanniferous forage plants to lambs artificially infected with Haemonchus contortus and Cooperia curticei. Veterinary Parasitology 146, 123–134.Google Scholar
Hedqvist, H, Mueller-Harvey, I, Reed, JD, Krueger, CG and Murphy, M (2000) Characterisation of tannins and in vitro protein digestibility of several Lotus corniculatus varieties. Animal Feed Science and Technology 87, 41–56.Google Scholar
Hernández-Villegas, MM, Borges-Argáez, R, Rodriguez-Vivas, RI, Torres-Acosta, JFJ, Méndez-Gonzalez, M and Cáceres-Farfan, M (2011) Ovicidal and larvicidal activity of the crude extracts from Phytolacca icosandra against Haemonchus contortus. Veterinary Parasitology 179, 100–106.Google Scholar
Hoste, H, Jackson, F, Athanasiadou, S, Thamsborg, SM and Hoskin, SO (2006) The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends in Parasitology 22, 253–261.Google Scholar
Howell, AB, Reed, JD, Krueger, CG, Winterbottom, R, Cunningham, DG and Leahy, M (2005) A-type cranberry proanthocyanidins and uropathogenic bacterial anti-adhesion activity. Phytochemistry 66, 2281–2291.Google Scholar
Katiki, LM, Ferreira, JF, Gonzalez, JM, Zajac, AM, Lindsay, DS, Chagas, ACS and Amarante, AF (2013) Anthelmintic effect of plant extracts containing condensed and hydrolyzable tannins on Caenorhabditis elegans, and their antioxidant capacity. Veterinary Parasitology 192, 218–227.Google Scholar
Kommuru, DS, Barker, T, Desai, S, Burke, JM, Ramsay, A, Mueller-Harvey, I, Miller, JE, Mosjidis, JA, Kamisetti, N and Terrill, TH (2014) Use of pelleted sericea lespedeza (Lespedeza cuneata) for natural control of coccidia and gastrointestinal nematodes in weaned goats. Veterinary Parasitology 204, 191–198.Google Scholar
Kommuru, DS, Whitley, NC, Miller, JE, Mosjidis, JA, Burke, JM, Gujja, S, Mechineni, A and Terrill, TH (2015) Effect of sericea lespedeza leaf meal pellets on adult female Haemonchus contortus in goats. Veterinary Parasitology 207, 170–175.Google Scholar
Kraus, TEC, Yu, Z, Preston, CM, Dahlgren, RA and Zasoski, RJ (2003) Linking chemical reactivity and protein precipitation to structural characteristics of foliar tannins. Journal of Chemical Ecology 29, 703–730.Google Scholar
Krueger, CG, Chesmore, N, Chen, X, Parker, J, Khoo, C, Marais, JP, Shanmuganayagam, D, Crump, P and Reed, JD (2016) Critical reevaluation of the 4-(dimethylamino) cinnamaldehyde assay: cranberry proanthocyanidin standard is superior to procyanidin A2 dimer for accurate quantification of proanthocyanidins in cranberry products. Journal of Functional Foods 22, 13–19.Google Scholar
Lange, KC, Olcott, DD, Miller, JE, Mosjidis, JA, Terrill, TH, Burke, JM and Kearney, MT (2006) Effect of sericea lespedeza (Lespedeza cuneata) fed as hay, on natural and experimental Haemonchus contortus infections in lambs. Veterinary Parasitology 141, 273–278.Google Scholar
Malisch, CS, Luscher, A, Baert, N, Engstrom, MT, Studer, B, Fryganas, C, Suter, D, Mueller-Harvey, I and Salminen, JP (2015) Large variability of proanthocyanidin content and composition in sainfoin (Onobrychis viciifolia). Journal of Agricultural and Food Chemistry 63, 10234–10242.Google Scholar
Marie-Magdeleine, C, Hoste, H, Mahieu, M, Varo, H and Archimede, H (2009) In vitro effects of Cucurbita moschata seed extracts on Haemonchus contortus. Veterinary Parasitology 161, 99–105.Google Scholar
Marley, CL, Cook, R, Keatinge, R, Barrett, J and Lampkin, NH (2003) The effect of birdsfoot trefoil (Lotus corniculatus) and chicory (Cichorium intybus) on parasite intensities and performance of lambs naturally infected with helminth parasites. Veterinary Parasitology 112, 147–155.Google Scholar
Mengistu, G, Hoste, H, Karonen, M, Salminen, JP, Hendriks, WH and Pellikaan, WF (2017) The in vitro anthelmintic properties of browse plant species against Haemonchus contortus is determined by the polyphenol content and composition. Veterinary Parasitology 237, 110–116.Google Scholar
Min, B, Pinchak, W, Anderson, R, Fulford, J and Puchala, R (2006) Effects of condensed tannins supplementation level on weight gain and in vitro and in vivo bloat precursors in steers grazing winter wheat. Journal of Animal Science 84, 2546–2554.Google Scholar
Molan, AL and Faraj, AM (2010) The effects of condensed tannins extracted from different plant species on egg hatching and larval development of Teladorsagia circumcincta (Nematoda: Trichostrongylidae). Folia Parasitologica 57, 62–68.Google Scholar
Molan, AL, Waghorn, GC, Min, BR and McNabb, WC (2000) The effect of condensed tannins from seven herbages on Trichostrongylus colubriformis larval migration in vitro. Folia Parasitologica 47, 39–44.Google Scholar
Molan, AL, Waghorn, GC and McNabb, WC (2002) Effect of condensed tannins on egg hatching and larval development of Trichostrongylus colubriformis in vitro. The Veterinary Record 150, 65–69.Google Scholar
Molan, AL, Meagher, LP, Spencer, PA and Sivakumaran, S (2003) Effect of flavan-3-ols on in vitro egg hatching, larval development and viability of infective larvae of Trichostrongylus colubriformis. International Journal for Parasitology 33, 1691–1698.Google Scholar
Monteiro, MVB, Bevilaqua, CML, Morais, SM, Machado, LKA, Camurça-Vasconcelos, ALF, Campello, CC, Ribeiro, WLC and Mesquita, MDA (2011) Anthelmintic activity of Jatropha curcas L. seeds on Haemonchus contortus. Veterinary Parasitology 182, 259–263.Google Scholar
Mueller-Harvey, I (2006) Unravelling the conundrum of tannins in animal nutrition and health. Journal of the Science of Food and Agriculture 86, 2010–2037.Google Scholar
Niezen, JH, Robertson, HA, Waghorn, GC and Charleston, WA (1998) Production, faecal egg counts and worm burdens of ewe lambs which grazed six contrasting forages. Veterinary Parasitology 80, 15–27.Google Scholar
Quijada, J, Fryganas, C, Ropiak, HM, Ramsay, A, Mueller-Harvey, I and Hoste, H (2015) Anthelmintic activities against Haemonchus contortus or Trichostrongylus colubriformis from small ruminants are influenced by structural features of condensed tannins. Journal of Agricultural and Food Chemistry 63, 6346–6354.Google Scholar
Roberts, C, Beuselinck, P, Ellersieck, M, Davis, D and McGraw, R (1993) Quantification of tannins in birdsfoot trefoil germplasm. Crop Science 33, 675–679.Google Scholar
Shaik, SA, Terrill, TH, Miller, JE, Kouakou, B, Kannan, G, Kaplan, RM, Burke, JM and Mosjidis, JA (2006) Sericea lespedeza hay as a natural deworming agent against gastrointestinal nematode infection in goats. Veterinary Parasitology 139, 150–157.Google Scholar
Skantar, AM, Agama, K, Meyer, SL, Carta, LK and Vinyard, BT (2005) Effects of geldanamycin on hatching and juvenile motility in Caenorhabditis elegans and Heterodera glycines. Journal of Chemical Ecology 31, 2481–2491.Google Scholar
Steiner, J, Beuselinck, P, Greene, S, Kamm, J, Kirkbride, J and Roberts, C (2001) A description and interpretation of the NPGS birdsfoot trefoil core subset collection. Crop Science 41, 1968–1980.Google Scholar
Terrill, TH, Waghorn, GC, Woolley, DJ, McNabb, WC and Barry, TN (1994) Assay and digestion of 14C-labelled condensed tannins in the gastrointestinal tract of sheep. The British Journal of Nutrition 72, 467–477.Google Scholar
USDA Agricultural Research Service, U.S. Department of Agriculture. (2014). Germplasm Resource Information Network (GRIN). (dataset) Ag Data Commons. doi: 10.15482/USDA.ADC/1212393 [doi].Google Scholar
Veríssimo, CJ, Niciura, SCM, Alberti, ALL, Rodrigues, CFC, Barbosa, CMP, Chiebao, DP, Cardoso, D, da Silva, GS, Pereira, JR, Margatho, LFF, da Costa, RLD, Nardon, RF, Ueno, TEH, Curci, VCLM and Molento, MB (2012) Multidrug and multispecies resistance in sheep flocks from São Paulo state, Brazil. Veterinary Parasitology 187, 209–216.Google Scholar
Waterman, PJ and Mole, S (1994) Analysis of Phenolic Plant Metabolites. London: Blackwell Scientific Publications.Google Scholar
Supplementary material: File

Barone et al. supplementary material

Table S1

Download Barone et al. supplementary material(File)
File 13.9 KB