Effect of Grape Pomace Inclusion in the Diet of Ewes Naturally Infected with Gastrointestinal Nematodes During Lactation
Abstract
:1. Introduction
2. Materials and Methods
2.1. Location, Animals, and Experimental Design
2.2. Grape Pomace Preparation
2.3. Measurement of Total Phenolics and Tannins in Grape Pomace
2.4. Fecal Sample Collection and Coprological Exams
2.5. Hematological Analyses
2.6. Anti-H. contortus L3 Immunoglobulin G (IgG)
2.7. Bromatological Analyses
2.8. Weight Gain
2.9. Meteorological Data
2.10. Statistical Analysis
3. Results
3.1. Dietary Nutrients
3.2. Fecal Examination
3.3. Coproculture
3.4. Packed Cell Volume and Total Plasma Protein
3.5. Blood Eosinophil Count and Anti-H. contortus L3 IgG Analysis
3.6. Body Weight of Lambs
3.7. Meteorological Data
4. Discussion
5. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Idris, A.; Moors, E.; Sohnrey, B.; Gauly, M. Gastrointestinal Nematode Infections in German Sheep. Parasitol. Res. 2012, 110, 1453–1459. [Google Scholar] [CrossRef] [PubMed]
- de Chagas, A.C.S.; Tupy, O.; dos Santos, I.B.; Esteves, S.N. Economic Impact of Gastrointestinal Nematodes in Morada Nova Sheep in Brazil. Rev. Bras. Parasitol. Veterinaria 2022, 31, e008722. [Google Scholar] [CrossRef]
- Toscano, J.H.B.; Lopes, L.G.; Giraldelo, L.A.; da Silva, M.H.; Okino, C.H.; de Souza Chagas, A.C. Identification of Appropriate Reference Genes for Local Immune-Related Studies in Morada Nova Sheep Infected with Haemonchus contortus. Mol. Biol. Rep. 2018, 45, 1253–1262. [Google Scholar] [CrossRef] [PubMed]
- Taylor, E.L. Seasonal Fluctuation in the Number of Eggs of Trichostrongylid Worms in the Faeces of Ewes. J. Parasitol. 1935, 21, 175. [Google Scholar] [CrossRef]
- O’Sullivan, B.M.; Donald, A.D. A Field Study of Nematode Parasite Populations in the Lactating Ewe. Parasitology 1970, 61, 301–315. [Google Scholar] [CrossRef]
- O’Sullivan, B.M.; Donald, A.D. Responses to Infection with Haemonchus contortus and Trichostrongylus colubriformis in Ewes of Different Reproductive Status. Int. J. Parasitol. 1973, 3, 521–530. [Google Scholar] [CrossRef]
- Houdijk, J.G.M.; Kyriazakis, I.; Jackson, F.; Huntley, J.F.; Coop, R.L. Is the Allocation of Metabolisable Protein Prioritised to Milk Production Rather than to Immune Functions in Teladorsagia circumcincta-Infected Lactating Ewes? Int. J. Parasitol. 2003, 33, 327–338. [Google Scholar] [CrossRef]
- Bricarello, P.A.; Gennari, S.M.; Oliveira-Sequeira, T.C.G.; Vaz, C.M.S.L.; Gonçalves de Gonçalves, I.; Echevarria, F.A.M. Worm Burden and Immunological Responses in Corriedale and Crioula Lanada Sheep Following Natural Infection with Haemonchus contortus. Small Rumin. Res. 2004, 51, 75–83. [Google Scholar] [CrossRef]
- Rocha, R.A.; Bricarello, P.A.; Silva, M.B.; Houdijk, J.G.M.; Almeida, F.A.; Cardia, D.F.F.; Amarante, A.F.T. Influence of Protein Supplementation during Late Pregnancy and Lactation on the Resistance of Santa Ines and Ile de France Ewes to Haemonchus contortus. Vet. Parasitol. 2011, 181, 229–238. [Google Scholar] [CrossRef]
- Flay, K.J.; Hill, F.I.; Muguiro, D.H. A Review: Haemonchus contortus Infection in Pasture-Based Sheep Production Systems, with a Focus on the Pathogenesis of Anaemia and Changes in Haematological Parameters. Animals 2022, 12, 1238. [Google Scholar] [CrossRef]
- Naeem, M.; Iqbal, Z.; Roohi, N. Ovine Haemonchosis: A Review. Trop. Anim. Health Prod. 2021, 53, 19. [Google Scholar] [CrossRef] [PubMed]
- Emery, D.L.; Hunt, P.W.; Le Jambre, L.F. Haemonchus contortus: The Then and Now, and Where to from Here? Int. J. Parasitol. 2016, 46, 755–769. [Google Scholar] [CrossRef] [PubMed]
- Cardia, D.F.F.; Rocha-Oliveira, R.A.; Tsunemi, M.H.; Amarante, A.F.T. Immune Response and Performance of Growing Santa Ines Lambs to Artificial Trichostrongylus colubriformis Infections. Vet. Parasitol. 2011, 182, 248–258. [Google Scholar] [CrossRef] [PubMed]
- Andronicos, N.M.; McNally, J.; Kotze, A.C.; Hunt, P.W.; Ingham, A. Trichostrongylus colubriformis Larvae Induce Necrosis and Release of IL33 from Intestinal Epithelial Cells in Vitro: Implications for Gastrointestinal Nematode Vaccine Design. Int. J. Parasitol. 2012, 42, 295–304. [Google Scholar] [CrossRef]
- Amarante, A.F.T. Controle de Verminose. Revista CFMV 2005, 11, 19–30. [Google Scholar]
- Satish, A.C.; Nagarajan, K.; Balachandran, C.; Soundararajan, C.; Legadevi, R. Gross, Histopathology and Molecular Diagnosis of Oesophagostomosis in Sheep. J. Parasit. Dis. 2018, 42, 315–320. [Google Scholar] [CrossRef]
- Bassetto, C.C.; Albuquerque, A.C.A.; Lins, J.G.G.; Marinho-Silva, N.M.; Chocobar, M.L.E.; Bello, H.J.S.; Mena, M.O.; Niciura, S.C.M.; Amarante, A.F.T.; Chagas, A.C.S. Revisiting Anthelmintic Resistance in Sheep Flocks from São Paulo State, Brazil. Int. J. Parasitol. Drugs Drug Resist. 2024, 24, 100527. [Google Scholar] [CrossRef]
- Sykes, A.; Coop, R.L. Interaction between Nutrition and Gastrointestinal Parasitism in Sheep. N Z Vet. J. 2001, 49, 222–226. [Google Scholar] [CrossRef]
- Knox, M.R.; Torres-Acosta, J.F.J.; Aguilar-Caballero, A.J. Exploiting the Effect of Dietary Supplementation of Small Ruminants on Resilience and Resistance against Gastrointestinal Nematodes. Vet. Parasitol. 2006, 139, 385–393. [Google Scholar] [CrossRef]
- Torres-Acosta, J.F.J.; Hoste, H. Alternative or Improved Methods to Limit Gastro-Intestinal Parasitism in Grazing Sheep and Goats. Small Rumin. Res. 2008, 77, 159–173. [Google Scholar] [CrossRef]
- Kalli, E.; Lappa, I.; Bouchagier, P.; Tarantilis, P.A.; Skotti, E. Novel Application and Industrial Exploitation of Winery By-Products. Bioresour. Bioprocess 2018, 5, 46. [Google Scholar] [CrossRef]
- Tayengwa, T.; Mapiye, C. Citrus and Winery Wastes: Promising Dietary Supplements for Sustainable Ruminant Animal Nutrition, Health, Production, and Meat Quality. Sustainability 2018, 10, 3718. [Google Scholar] [CrossRef]
- Machado, A.R.; Voss, G.B.; Machado, M.; Paiva, J.A.P.; Nunes, J.; Pintado, M. Chemical Characterization of the Cultivar ‘Vinhão’ (Vitis vinifera L.) Grape Pomace towards Its Circular Valorisation and Its Health Benefits. Meas. Food 2024, 15, 100175. [Google Scholar] [CrossRef]
- Popovici, V.; Boldianu, A.-B.; Pintea, A.; Caraus, V.; Ghendov-Mosanu, A.; Subotin, I.; Druta, R.; Sturza, R. In Vitro Antioxidant Activity of Liposomal Formulations of Sea Buckthorn and Grape Pomace. Foods 2024, 13, 2478. [Google Scholar] [CrossRef]
- Soares, S.C.S.; Lima, G.C.; Laurentiz, A.C.; Féboli, A.; Anjos, L.A.; Carlis, M.S.P.; Filardi, R.S.; Laurentiz, R.S. In Vitro Anthelmintic Activity of Grape Pomace Extract Against Gastrointestinal Nematodes of Naturally Infected Sheep. Int. J. Vet. Sci. Med. 2018, 6, 243–247. [Google Scholar] [CrossRef]
- Mena, M.O.; Trevise, G.G.O.; Silva, T.N.R.; Moellmann, V.M.; Bassetto, C.C.; Gatti, B.S.; Louvandini, H.; Soutello, R.V.G.; Albuquerque, A.C.A.; Amarante, A.F.T. Evaluation of Grape Pomace Supplementation in Lamb Diets to Mitigate Haemonchus contortus Infection. Agriculture 2025, 15, 341. [Google Scholar] [CrossRef]
- Makkar, H.P.S. Quantification of Tannins in Tree and Shrub Foliage; Springer Netherlands: Dordrecht, The Netherlands, 2003. [Google Scholar] [CrossRef]
- Makkar, H.P.S.; Blümmel, M.; Borowy, N.K.; Becker, K. Gravimetric Determination of Tannins and Their Correlations with Chemical and Protein Precipitation Methods. J. Sci. Food Agric. 1993, 61, 161–165. [Google Scholar] [CrossRef]
- Ueno, H.; Gonçalves, P.C. Manual Para Diagnóstico Das Helmintoses de Ruminantes, 4th ed.; JICA: Tokyo, Japan, 1998. [Google Scholar]
- Dawkins, H.J.S.; Windon, R.G.; Eagleson, G.K. Eosinophil Responses in Sheep Selected for High and Low Responsiveness to Trichostrongylus colubriformis. Int. J. Parasitol. 1989, 19, 199–205. [Google Scholar] [CrossRef]
- Amarante, A.F.T.; Susin, I.; Rocha, R.A.; Silva, M.B.; Mendes, C.Q.; Pires, A.V. Resistance of Santa Ines and Crossbred Ewes to Naturally Acquired Gastrointestinal Nematode Infections. Vet. Parasitol. 2009, 165, 273–280. [Google Scholar] [CrossRef]
- Silva, B.F.; Bassetto, C.C.; Amarante, A.F.T. Immune Responses in Sheep Naturally Infected with Oestrus ovis (Diptera: Oestridae) and Gastrointestinal Nematodes. Vet. Parasitol. 2012, 190, 120–126. [Google Scholar] [CrossRef]
- Santos, M.C.; Xavier, J.K.; Amarante, M.R.V.; Bassetto, C.C.; Amarante, A.F.T. Immune Response to Haemonchus contortus and Haemonchus placei in Sheep and Its Role on Parasite Specificity. Vet. Parasitol. 2014, 203, 127–138. [Google Scholar] [CrossRef] [PubMed]
- Kanobana, K.; Vervelde, L.; Van Der Veer, M.; Eysker, M.; Ploeger, H.W. Characterization of Host Responder Types after a Single Cooperia oncophora Infection: Kinetics of the Systemic Immune Response. Parasite Immunol. 2001, 23, 641–653. [Google Scholar] [CrossRef] [PubMed]
- AOAC International. Official Methods of Analysis of AOAC International, 20th ed.; AOAC International: Washington, DC, USA, 2016. [Google Scholar]
- Van Soest, P.J.; Robertson, J.B.; Lewis, B.A. Methods for Dietary Fiber, Neutral Detergent Fiber, and Nonstarch Polysaccharides in Relation to Animal Nutrition. J. Dairy Sci. 1991, 74, 3583–3597. [Google Scholar] [CrossRef] [PubMed]
- Mertens, D.R. Gravimetric Determination of Amylase-Treated Neutral Detergent Fiber in Feeds with Refluxing in Beakers or Crucibles: Collaborative Study. J. AOAC Int. 2002, 85, 1217–1240. [Google Scholar] [CrossRef]
- López-Leyva, Y.; González-Garduño, R.; Cruz-Tamayo, A.A.; Arece-García, J.; Huerta-Bravo, M.; Ramírez-Valverde, R.; Torres-Hernández, G.; López-Arellano, M.E. Protein Supplementation as a Nutritional Strategy to Reduce Gastrointestinal Nematodiasis in Periparturient and Lactating Pelibuey Ewes in a Tropical Environment. Pathogens 2022, 11, 941. [Google Scholar] [CrossRef]
- Beasley, A.M.; Kahn, L.P.; Windon, R.G. The Periparturient Relaxation of Immunity in Merino Ewes Infected with Trichostrongylus colubriformis: Parasitological and Immunological Responses. Vet. Parasitol. 2010, 168, 60–70. [Google Scholar] [CrossRef]
- Li, X.; Xiang, H.; Liang, R.; Han, X.; Zhong, R.; Liu, H.; Fang, Y. Tannin Alleviated Reproductive Dysfunction in Pregnant Ewes Infected with Haemonchus contortus. Front. Vet. Sci. 2025, 12. [Google Scholar] [CrossRef]
- Kadigi, J.H.; Muzzo, B.I.; Schreiber, S. Potential Benefits of Tannins on Ruminant Health, Production and Environmental Sustainability. Eur. J. Nutr. Food Saf. 2024, 16, 13–24. [Google Scholar] [CrossRef]
- Almeida, F.A.; Albuquerque, A.C.A.; Bassetto, C.C.; Starling, R.Z.C.; Lins, J.G.G.; Amarante, A.F.T. Long Spelling Periods Are Required for Pasture to Become Free of Contamination by Infective Larvae of Haemonchus contortus in a Humid Subtropical Climate of São Paulo State, Brazil. Vet. Parasitol. 2020, 279, 109060. [Google Scholar] [CrossRef]
- Wilmsen, M.O.; Silva, B.F.; Bassetto, C.C.; do Amarante, A.F.T. Gastrointestinal Nematode Infections in Sheep Raised in Botucatu, State of São Paulo, Brazil. Rev. Bras. De Parasitol. Veterinária 2014, 23, 348–354. [Google Scholar] [CrossRef]
- Ortiz-Ocampo, G.I.; Torres-Acosta, J.F.J.; Sandoval-Castro, C.A.; Hoste, H.; Capetillo-Leal, C.M.; González-Pech, P.G.; Santos-Ricalde, R.H. In Vitro and in Vivo Anthelmintic Effect of Coffea Arabica Residues Againts an Haemonchus contortus Isolate with Low Susceptibility to Tannins. Trop. Subtrop. Agroecosystems 2016, 19, 41–50. [Google Scholar] [CrossRef]
- Lecasble, C. Le Marc de Cafe Comme Source Non Conventionnelle de Tanins Condenses Dans Le Controle Alternatif Des Nematodes Gastrointestinaux Chez Les Petits Ruminants Du Yucatan, Mexique. Ph.D. Thesis, École Nationale Vétérinaire de Toulouse, Toulouse, France, 2011. [Google Scholar]
- Dove, H.; Milne, J.A.; Lamb, C.S.; Sibbald, A.M.; McCormack, H.A. The Influence of Herbage Mass and Supplementary Feeding on Nutrient Flows and Animal Performance in Grazing, Lactating Ewes. J. Agric. Sci. 2012, 150, 644–662. [Google Scholar] [CrossRef]
- Reed, S.A.; Raja, J.S.; Hoffman, M.L.; Zinn, S.A.; Govoni, K.E. Poor Maternal Nutrition Inhibits Muscle Development in Ovine Offspring. J. Anim. Sci. Biotechnol. 2014, 5, 43. [Google Scholar] [CrossRef] [PubMed]
- Gauvin, M.C.; Pillai, S.M.; Reed, S.A.; Stevens, J.R.; Hoffman, M.L.; Jones, A.K.; Zinn, S.A.; Govoni, K.E. Poor Maternal Nutrition during Gestation in Sheep Alters Prenatal Muscle Growth and Development in Offspring. J. Anim. Sci. 2020, 98, skz388. [Google Scholar] [CrossRef]
- Calvillo-Marín, J.M.; Álvares-Fuentes, G.; García-López, J.C.; Rendón Huerta, J.A. Dry Brewer Grains as Replacement for Alfalfa in Diets for Lactating Ewes. Agrociencia 2022, 56. [Google Scholar] [CrossRef]
- Jalal, H.; Giammarco, M.; Lanzoni, L.; Akram, M.Z.; Mammi, L.M.E.; Vignola, G.; Chincarini, M.; Formigoni, A.; Fusaro, I. Potential of Fruits and Vegetable By-Products as an Alternative Feed Source for Sustainable Ruminant Nutrition and Production: A Review. Agriculture 2023, 13, 286. [Google Scholar] [CrossRef]
Groups | Type of Birth | Concentrate (kg) | Grape Pomace (kg) |
---|---|---|---|
Supplemented (n = 8) | Single (n = 5) | 0.8 | 0.2 |
Twin (n = 3) | 1.0 | 0.2 | |
Control (n = 10) | Single (n = 6) | 1.0 | 0 |
Twin (n = 4) | 1.2 | 0 |
Procedures | Days | |||||||||||||
---|---|---|---|---|---|---|---|---|---|---|---|---|---|---|
−38 * | −17 * | 0 | 7 | 14 | 21 | 28 | 35 | 42 | 49 | 56 | 63 | 77 | 91 | |
Prepartum sampling | X | X | ||||||||||||
Parturition day | X | |||||||||||||
Lactation sampling ** | X | X | X | X | X | X | X | X | X | |||||
Post-weaning sampling | X | X | ||||||||||||
Grape pomace feeding | X | X | X | X | X |
Variables (%) | Grape Pomace | Concentrate | Pasture |
---|---|---|---|
DM | 93.59 | 91.16 | 86.02 |
CP | 12.61 | 18.71 | 10.13 |
NDF | 45.42 | 17.17 | 72.03 |
ADF | 66.50 | 12.06 | 46.85 |
EE | 5.71 | 3.19 | 2.55 |
MM | 10.89 | 3.38 | 8.59 |
Total phenolic compounds a | 47.87 | - | - |
Total tannins a | 42.21 | - | - |
Condensed tannins b | 2.63 | - | - |
Period | Day | Supplemented (n = 8) | Control (n = 10) | p-Value |
---|---|---|---|---|
Prepartum | −38 # | 75.0 ± 36.60 | 260.0 ± 195.62 | 0.7507 |
−17 # | 1625.0 ± 649.38 | 520.0 ± 174.99 | 0.0864 | |
Lactation (Weekly sampling) | 7 * | 1662.5 ± 551.60 | 1790.0 ± 381.65 | 0.7943 |
14 * | 975.0 ± 413.50 | 2960.0 ± 1192.87 | 0.0087 | |
21 * | 725.0 ± 372.13 | 1970.0 ± 921.96 | 0.0856 | |
28 * | 762.5 ± 402.64 | 1370.0 ± 805.13 | 0.4305 | |
35 * | 475.0 ± 256.87 | 1200.0 ± 516.61 | 0.2520 | |
42 | 437.5 ± 155.77 | 1300.0 ± 587.08 | 0.1894 | |
49 | 237.5 ± 98.08 | 670.0 ± 255.63 | 0.4570 | |
56 | 337.5 ± 129.47 | 500.0 ± 197.77 | 0.7816 | |
63 | 250.0 ± 96.36 | 320.0 ± 121.84 | 0.9019 | |
Post-Weaning (Biweekly sampling) | 77 | 550.0 ± 281.58 | 440.0 ± 166.13 | 0.8616 |
91 | 437.5 ± 186.07 | 540.0 ± 260.00 | 0.8749 |
Weight | Supplemented (n = 11) | Control (n = 12) | p-Value | ||||
---|---|---|---|---|---|---|---|
Single (5) | Twin (6) | Single (7) | Twin (5) | Type of Birth | Group | Type of Birth × Group | |
Birth | 4.2 ± 0.42 | 3.4 ± 0.24 | 4.6 ± 0.33 | 3.8 ± 0.24 | 0.0193 | 0.2675 | 0.7602 |
Weaning | 19.5 ± 1.29 | 15.2 ± 1.65 | 18.2 ± 0.73 | 11.8 ± 1.62 | 0.0008 | 0.0942 | <0.0001 |
Weight gain | 15.2 ± 0.94 | 11.8 ± 1.60 | 13.6 ± 0.77 | 8.0 ± 1.83 | 0.0029 | 0.0539 | 0.4394 |
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Mena, M.O.; Trevise, G.G.d.O.; Bassetto, C.C.; Pinchao, W.H.P.; Louvandini, H.; Soutello, R.V.G.d.; Albuquerque, A.C.A.; Amarante, A.F.T.d. Effect of Grape Pomace Inclusion in the Diet of Ewes Naturally Infected with Gastrointestinal Nematodes During Lactation. Pathogens 2025, 14, 560. https://doi.org/10.3390/pathogens14060560
Mena MO, Trevise GGdO, Bassetto CC, Pinchao WHP, Louvandini H, Soutello RVGd, Albuquerque ACA, Amarante AFTd. Effect of Grape Pomace Inclusion in the Diet of Ewes Naturally Infected with Gastrointestinal Nematodes During Lactation. Pathogens. 2025; 14(6):560. https://doi.org/10.3390/pathogens14060560
Chicago/Turabian StyleMena, Mateus Oliveira, Gustavo Gabriel de Oliveira Trevise, César Cristiano Bassetto, Willinton Hernan Pinchao Pinchao, Helder Louvandini, Ricardo Velludo Gomes de Soutello, Ana Cláudia Alexandre Albuquerque, and Alessandro Francisco Talamini do Amarante. 2025. "Effect of Grape Pomace Inclusion in the Diet of Ewes Naturally Infected with Gastrointestinal Nematodes During Lactation" Pathogens 14, no. 6: 560. https://doi.org/10.3390/pathogens14060560
APA StyleMena, M. O., Trevise, G. G. d. O., Bassetto, C. C., Pinchao, W. H. P., Louvandini, H., Soutello, R. V. G. d., Albuquerque, A. C. A., & Amarante, A. F. T. d. (2025). Effect of Grape Pomace Inclusion in the Diet of Ewes Naturally Infected with Gastrointestinal Nematodes During Lactation. Pathogens, 14(6), 560. https://doi.org/10.3390/pathogens14060560