Abstract
Purpose
Some agroindustrial by-products could be used as nutraceutical materials for small ruminants helping with their nutrition while controlling their gastrointestinal nematodes. This study evaluated the potential in vitro nutraceutical value of pod husks and leaves of three varieties of Theobroma cacao using two Haemonchus contortus isolates with different polyphenol susceptibility.
Methods
Leaves and husks from three T. cacao varieties (AZT, CAL and CEY) were evaluated for their bromatological composition, in vitro dry matter digestibility and polyphenol content. Acetone:water extracts (70:30) of each plant variety were evaluated using the egg hatch and larval exsheathment inhibition tests, using two isolates (FESC and PARAISO) of H. contortus. Effective concentrations 50% (EC50) were determined for both tests. The role of polyphenols was confirmed using polyvinylpolypyrrolidone. L3 exposed to CAL leaf extract were submitted to transmission electron microscopy.
Results
Both plant materials showed a good nutritional value to complement protein-rich diets for small ruminants. Extracts inhibited exsheathment of H. contortus L3 more effectively than the egg hatching, and the leaf extracts were more active than husk extracts in the L3 exsheathment inhibition. The FESC isolate was more sensitive to extracts. Polyphenols blocked exsheathment inhibition of leaf extracts. Structural damage was observed in the sheath and muscles of L3 exposed to CAL leaf extracts.
Conclusion
The two T. cacao materials tested showed their potential to be used as ruminant feeds. Extracts affected H. contortus by blocking L3 exsheathment, particularly with the leaf extracts. The in vivo nutraceutical value should be confirmed in small ruminants.
Similar content being viewed by others
Data availability
The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.
Code availability
Not applicable.
References
Torres-Acosta JFJ, Hoste H, Sandoval-Castro CA, Torres-Fajardo RA, Ventura-Cordero J, González-Pech PG, Mancilla-Montelongo MG, Ojeda-Robertos NF, Martínez-Ortíz-de-Montellano C (2019) The “Art of War” against gastrointestinal nematodes in sheep and goat herds of the tropics. Rev Acad 17(S1):39–46
Hoste H, Torres-Acosta JFJ, Quijada J, Chan-Pérez I, Dakheel MM, Kommuru DS, Mueller-Harvey I, Terrill TH (2016) Interactions between nutrition and infections with Haemonchus contortus and related gastrointestinal nematodes in small ruminants. Adv Parasitol 93:239–351. https://doi.org/10.1016/bs.apar.2016.02.025
Hoste H, Torres-Acosta JFJ, Sandoval-Castro CA, Terril T, Sotiraki S, Thamsborg S, Louvandini H, Costa-Junior LM, Mueller-Harvey I (2018) Tannin containing plants vs synthetic anthelmintics to control gastrointestinal nematodes in small ruminants: an upside down approach. In: Beltrao-Molento M, Miller J (eds) Novel approaches to the control of helminth parasites of livestock: facing the challenge of helminths infections in tropical and subtropical areas, 1st edn. Appris, Curitiba, Brasil, pp 71–80
Hoste H, Jackson F, Athanasiadou S, Thamsborg SM, Hoskin SO (2006) The effects of tannin-rich plants on parasitic nematodes in ruminants. Trends Parasitol 22:253–261. https://doi.org/10.1016/j.pt.2006.04.004
Castañeda-Ramírez GS, Rodríguez-Labastida M, Ortiz-Ocampo GI, González-Pech PG, Ventura-Cordero J, Borges-Argáez R, Torres-Acosta JFJ, Sandoval-Castro CA, Mathieu C (2018) An in vitro approach to evaluate the nutraceutical value of plant foliage against Haemonchus contortus. Parasitol Res 117:3979–3991. https://doi.org/10.1007/s00436-018-6107-0
Méndez-Ortiz FA, Sandoval-Castro CA, Ventura-Cordero J, Sarmiento-Franco LA, Santos-Ricalde RH, Torres-Acosta JFJ (2019) Gymnopodium floribundum fodder as a model for the in vivo evaluation of nutraceutical value against Haemonchus contortus. Trop Anim Health Prod 51:1591–1599. https://doi.org/10.1007/s11250-019-01855-9
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 212:5–17. https://doi.org/10.1016/j.vetpar.2015.06.026
Vargas-Magaña JJ, Torres-Acosta JFJ, Aguilar-Caballero AJ, SandovalCastro CA, Hoste H, Perez JI (2014) Anthelmintic activity of acetone-water extracts against Haemonchus contortus eggs: interactions between tannins and other plant secondary compounds. Vet Parasitol 206:322–327. https://doi.org/10.1016/j.vetpar.2014.10.008
Cádiz-Gurrea MDLL, Borrás-Linares I, Lozano-Sánchez J, Joven J, Fernández-Arroyo S, Segura-Carretero A (2017) Cocoa and grape seed byproducts as a source of antioxidant and anti-inflammatory proanthocyanidins. Int J Mol Sci 18:376. https://doi.org/10.3390/ijms18020376
Campos-Vega R, Nieto-Figueroa KH, Oomah BD (2018) Cocoa (Theobroma cacao L.) pod husk: renewable source of bioactive compounds. Trends Food Sci Tech 81:172–184. https://doi.org/10.1016/j.tifs.2018.09.022
Castillo-Mitre GF, Olmedo-Juárez A, Rojo-Rubio R, González-Cortázar M, Mendoza-de Gives P, Hernández-Beteta EE, Reyes-Guerrero DE, López-Arellano ME, Vázquez-Armijo JF, Ramírez-Vargas G, Zamilpa A (2017) Caffeoyl and coumaroyl derivatives from Acacia cochliacantha exhibit ovicidal activity against Haemonchus contortus. J Ethnopharmacol 204:125–131. https://doi.org/10.1016/j.jep.2017.04.010
Ashihara H, Suzuki T (2004) Distribution and biosynthesis of caffeine in plants. Front Biosci 9:1864–1876. https://doi.org/10.2741/1367
Hernández-Hernández C, Viera-Alcaide I, Morales-Sillero AM, Fernández-Bolaños J, Rodríguez-Gutiérrez G (2018) Bioactive compounds in Mexican genotypes of cocoa cotyledon and husk. Food Chem 240:831–839. https://doi.org/10.1016/j.foodchem.2017.08.018
FAO (Food and Agriculture Organization of the United Nations) (1977) Cocoa, 3rd edn. Better Farming series, Rome, Italy
Baharum Z, Akim AM, Taufiq-Yap YH, Hamid RA, Kasran R (2014) in vitro antioxidant and antiproliferative activities of methanolic plant part extracts of Theobroma cacao. Molecules 19:18317–18331. https://doi.org/10.3390/molecules191118317
Chan-Pérez JI, Torres-Acosta JFJ, Sandoval-Castro CA, Hoste H, Castañeda-Ramírez GS, Mathieu C, Vilarem G (2016) In vitro susceptibility of ten Haemonchus contortus isolates from different geographical origins towards acetone:water extracts of two tannin rich plants. Vet Parasitol 217:53–60. https://doi.org/10.1016/j.vetpar.2015.11.001
Sandoval-Castro CA, Torres-Acosta JFJ, Hoste H, Salem AZM, Chan-Pérez JI (2012) Using plant bioactive materials to control gastrointestinal tract helminths in livestock. Anim Feed Sci Tech 176:192–201. https://doi.org/10.1016/j.anifeedsci.2012.07.023
Chan-Pérez JI, Torres-Acosta JFJ, Sandoval-Castro CA, Castañeda-Ramírez GS, Vilarem G, Mathieu C, Hoste H (2017) Susceptibility of ten Haemonchus contortus isolates from different geographical origins towards acetone: water extracts of polyphenol-rich plants. Part 2: Infective L3 larvae. Vet Parasitol 240:11–16. https://doi.org/10.1016/j.vetpar.2017.04.023
Bowman DD, Lynn RC (1999) Georgis´ parasitology for veterinarians, 7th edn. WB Saunders, Philadelphia
Ministry of Agriculture, Fisheries and Food (MAFF) (1986) Manual of veterinary parasitological laboratory techniques (Reference Book; 418), 3rd edn. Her Majesty's Stationery Office (HMSO), London.
Castañeda-Ramírez GS, Mathieu C, Vilarem G, Hoste H, Mendoza-de Gives P, González-Pech PG, Torres-Acosta JFJ, Sandoval-Castro CA (2017) Age of Haemonchus contortus third stage infective larvae is a factor influencing the in vitro assessment of anthelmintic properties of tannin containing plant extracts. Vet Parasitol 243:130–134. https://doi.org/10.1016/j.vetpar.2017.06.019
von Samson-Himmelstjerna G, Coles GC, Jackson F, Bauer C, Borgsteede F, Cirak VY, Demeler J, Donnan A, Dorny P, Epe C, Harder A, Höglund J, Kaminsky R, Kerboeuf D, Küttler U, Papadopoulos E, Posedi J, Small J, Várady M, Vercruysse J, Wirtherle N (2009) Standardization of the egg hatch test for the detection of benzimidazole resistance in parasitic nematodes. Parasitol Res 105:825–834. https://doi.org/10.1007/s00436-009-1466-1
Jackson F, Hoste H (2010) In vitro methods for the primary screening of plant products for direct activity against ruminant gastrointestinal nematodes. In: Vercoe PE, Makkar HPS, Schlink AC (eds) In vitro screening of plant resource for extra-nutritional attributes in ruminants: nuclear and related methodologies. Springer Science+Business Media B.V., Dordrecht, pp 25–45. Doi: https://doi.org/10.1007/978-90-481-3297-3_3
Makkar HP, Blümmel M, Becker K (1995) Formation of complexes between polyvinyl pyrrolidones or polyethylene glycols and tannins, and their implication in gas production and true digestibility in in vitro techniques. Br J Nutr 73:897–913. https://doi.org/10.1079/BJN19950095
AOAC (1980) Oficial methods of analysis, 13th edn. Association of Official Analytical Chemists, Washington
Thiex NJ, Anderson S, Gildemeister B (2003) Crude fat, diethyl ether extraction, in feed, cereal grain, and forage randall/soxtec/submersion method): collaborative study. J AOAC Int 86:888–898. https://doi.org/10.1093/jaoac/86.5.888
Mertens DR (2002) Gravimetric determination of amylase-treated neutral detergent fiber in feeds with refluxing in beakers or crucibles: collaborative study. J AOAC Int 85:1217–1240
Van Soest PJ, Robertson JB, Lewis BA (1991) Methods for dietary fiber, neutral detergent fiber, and nonstarch polysaccharides in relation to animal nutrition. J Dairy Sci 74:3583–3597. https://doi.org/10.3168/jds.S0022-0302(91)78551-2
Robertson JB, Van Soest PJ (1981) The detergent system of analysis and its application to human. In: James WPT, Theander O (eds) The analysis of dietary fiber in food. Marcel Dekker, New York, pp 123–158
Makkar HP (2003) Quantification of tannins in tree and shrub foliage: a laboratory manual. Springer Science+Business Media, Berlin
Barros-Rodríguez M, Solorio-Sánchez J, Ku-Vera J, Ayala-Burgos A, Sandoval-Castro C, Solís-Pérez G (2012) Productive performance and urinary excretion of mimosine metabolites by hair sheep grazing in a silvopastoral system with high densities of Leucaena leucocephala. Trop Anim Health Prod 44:1873–1878. https://doi.org/10.1007/s11250-012-0150-0
AFRC (1993) Energy and protein requirements of ruminants. An advisory manual prepared by the AFRC. Technical Committee on Responses to Nutrients. CAB International, Wallingford, UK
Lock O, Cabello I, Doroteo VH (2006) Práctica VI. 6 Análisis de flavonoides en plantas analysis of flavonoids in plants. https://old.iupac.org/publications/cd/medicinal_chemistry/Practica-VI-6.pdf Accessed 10 July 2020
Mac Donald D, Valencia EF, Cuyos M, Dueñas R (2005) Extracción, identificación y evaluación de saponinas en Agaricus bisporus. Biotempo 5:3–36. https://doi.org/https://doi.org/10.31381/biotempo.v5i0.889
Harborne JB (1973) Phytochemical methods a guide to modern techniques of plant analysis. Springer, Dordrecht
Merck E (1974) Dyeing reagents for thin-layer and paper chromatography. KGaA, Darmstadt
Software LeOra (2004) Polo plus. Probit and logit analysis, LeOra Software, Berkeley
Jeske DR, Xu HK, Blessinger T (2009) Testing for the equality of EC50 values in the presence of unequal slopes with application to toxicity of selenium types. J Agric Biol Environ Stat 14:469–483. https://doi.org/10.1198/jabes.2009.07088
R Core Team (2018) R: a language and environment for statistical computing. R foundation for statistical computing, Vienna, Austria. https://www.R-project.org/
Ventura-Cordero J, González-Pech PG, Torres-Acosta JFJ, Sandoval-Castro CA, Tun-Garrido J (2019) Sheep and goat browsing a tropical deciduous forest during the rainy season: why does similar plant species consumption result in different nutrient intake? Anim Prod Sci 59:66–72. https://doi.org/10.1071/AN16512
González-Pech PG, Torres-Acosta JFJ, Sandoval-Castro CA, Tun-Garrido J (2015) Feeding behavior of sheep and goats in a deciduous tropical forest during the dry season: the same menu consumed differently. Small Ruminant Res 133:128–134. https://doi.org/10.1016/j.smallrumres.2015.08.020
Ayala-Burgos A, Cetina-Góngora R, Capetillo-Leal C, Zapata-Campos C, Sandoval-Castro C (2006) Composición química nutricional de árboles forrajeros. Compilación de análisis de laboratorio de nutrición animal. Universidad Autónoma de Yucatán, FMVZ, Mérida, Yucatán, México
Preston TR (1982) Nutritional limitations associated with the feeding of tropical forages. J Anim Sci 54:877–884. https://doi.org/10.2527/jas1982.544877x
Torres-Fajardo RA, González-Pech PG, Sandoval-Castro CA, Ventura-Cordero J, Torres-Acosta JFJ (2019) Criollo goats limit their grass intake in the early morning suggesting a prophylactic self-medication behaviour in a heterogeneous vegetation. Trop Anim Health Prod 51:2473–2479. https://doi.org/10.1007/s11250-019-01966-3
Ortíz-Ocampo GI, Torres-Acosta JFJ, Sandoval-Castro CA, Hoste H, Capetillo-Leal CM, González-Pech PG, Santos-Ricalde RH (2016) In vitro and in vivo anthelmintic effect of Coffea arabica residues against an Haemonchus contortus isolate with low susceptibility to tannins. Trop Subtrop Agroecosyst 19:41–50
Castañeda-Ramírez GS, Torres-Acosta JFJ, Sandoval-Castro CA, González-Pech PG, Parra-Tabla VP, Mathieu C (2017) Is there a negative association between the content of condensed tannins, total phenols and total tannins of tropical plant extracts and the in vitro anthelmintic activity against Haemonchus contortus eggs? Parasitol Res 116:3341–3348. https://doi.org/10.1007/s00436-017-5650-4
von Son-de FE, Alonso-Díaz MÁ, Valles-de la Mora B, Mendoza-de Gives P, Castillo-Gallegos E, Zamilpa A, González-Cortazar M (2018) Effect of Gliricidia sepium leaves intake on larval establishment of Cooperia punctata in calves and bio-guided fractionation of bioactive molecules. Vet Parasitol 252:137–141. https://doi.org/10.1016/j.vetpar.2018.02.003
Brunet S, Fourquaux I, Hoste H (2011) Ultrastructural changes in the third-stage, infective larvae of ruminant nematodes treated with sainfoin (Onobrychis viciifolia) extract. Parasitol Int 60:419–424. https://doi.org/10.1016/j.parint.2010.09.011
Mancilla G, Castañeda-Ramírez S, Borges-Argáez R, Cáceres-Farfán M, Sandoval-Castro C, Torres-Acosta F (2019) Evaluación fitoquímica preliminar de plantas tropicales con potencial nutracéutico para pequeños rumiantes. Rev Latinoamer Quim 47(Supl):71
Rue EA, Rush MD, van Breemen RB (2018) Procyanidins: a comprehensive review encompassing structure elucidation via mass spectrometry. Phytochem Rev 17:1–16. https://doi.org/10.1007/s11101-017-9507-3
Sánchez-Rabaneda F, Jáuregui O, Casals I, Andrés-Lacueva C, Izquierdo-Pulido M, Lamuela-Raventós RM (2003) Liquid chromatographic/electrospray ionization tandem mass spectrometric study of the phenolic composition of cocoa (Theobroma cacao). J Mass Spectrom 38:35–42. https://doi.org/10.1002/jms.395
Barrett A, Ndou T, Hughey CA, Straut C, Howell A, Dai Z, Kaletunc G (2013) Inhibition of α-amylase and glucoamylase by tannins extracted from cocoa, pomegranates, cranberries, and grapes. J Agr Food Chem 61:1477–1486. https://doi.org/10.1021/jf304876g
Acknowledgements
The authors thank the Dr. Alfredo Cuellar-Ordáz from the Facultad de Estudios Superiores Cuautitlán, Universidad Nacional Autónoma de México (FESC-UNAM) for providing the FESC Haemonchus contortus isolate. De La Cruz-Cortazar acknowledge the Consejo Nacional de Ciencia y Tecnología (CONACYT, México) for granting a scholarship to pursue a master’s degree. Mancilla-Montelongo thanks to Cátedras CONACYT Program (Project number 692) for the research fellowship.
Funding
This work was financed by the Consejo Nacional de Ciencia y Tecnología (CONACYT, México) project: CB-2013–01/221041. Also, this study was part of the international Postgraduate Cooperation Program between France and CONACYT, México (PCP-2013–229330).
Author information
Authors and Affiliations
Contributions
Conceptualization: JFT-A, CM, CAS-C, HH; methodology: GSC-R, JIC-P, GM-M; formal analysis and investigation: ÁDlC-C, MLC-V, GSC-R, JIC-P, EG, PGG-P, GM-M; resources: not applicable; writing—original draft preparation: GM-M; writing—review and editing: GM-M, JFT-A, CM, CAS-C, HH, JV-C, PGG-P, IF; funding acquisition: CM, HH, CAS-C, JFT-A; supervision: CM, CAS-C, HH, JFT-A.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
The authors assert that all procedures contributing to this work comply with the ethical standards of the relevant national and institutional guides on the care and use of laboratory animals. Approval was granted by the ethical standards of the Bioethics Committee of the Faculty of Veterinary Medicine and Animal Science, Universidad Autónoma de Yucatán (license No. CB-CCBA-D- 2014–003).
Consent to participate
Not applicable.
Consent for publication
Not applicable.
Rights and permissions
About this article
Cite this article
Mancilla-Montelongo, M.G., Castañeda-Ramírez, G.S., Gaudin-Barbier, E. et al. In vitro Evaluation of the Nutraceutical Potential of Theobroma cacao pod Husk and Leaf Extracts for Small Ruminants. Acta Parasit. 66, 1122–1136 (2021). https://doi.org/10.1007/s11686-021-00354-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11686-021-00354-y