Folia Parasitologica 71:009 (2024) | DOI: 10.14411/fp.2024.009

Effects of three kinds of Chinese herbs on growth performance, oocysts output and gut microbiota in growing lambs with coccidiosis

Yanfeng He1#, Zhanming Wang1#, Shijie Li1, Pan Chen1, Kaili Liu1, Manman Li2, Yingmin Wang2, Aftab Shaukat3, Muhammad Abdullah4, Senyang Li1, Shucheng Huang ORCID...1*, Fuchun Jian ORCID...1*
1 College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China;
2 Henan Zhongyang Animal Husbandry Co. Ltd., China;
3 National Center for International Research on Animal Genetics, Breeding and Reproduction (NCIRAGBR), Huazhong Agricultural University, Wuhan, China;
4 Cholistan Institute of Desert Studies, The Islamia University of Bahawalpur, Pakistan. # These authors contributed equally. *Corresponding author: Shucheng Huang, E-mail: huang.sc@henau.edu.cn, ORCID: 0000-0003-3163-8616; Fuchun Jian, E-mail: jfchun2008@163.com, ORCID: 0000-0001-9481-2277. Address for correspondence: College of Veterinary Medicine, Henan Agricultural University, Zhengzhou, China.

Coccidiosis is a protozoan intestinal disease that reduces the production of the sheep industry and causes large economic losses for sheep. Although chemically synthesised drugs are routinely employed to treat coccidiosis in sheep, the anticoccidial drug resistance and drug residues in edible meat have prompted an urgent search for alternatives. Herein, the anticoccidial properties of diclazuril, a conventional anticoccidial drug, and Allium sativum, Houttuynia cordata and Portulaca oleracea were assessed. Forty 45-day-old lambs naturally infected with Eimeria spp. were selected and randomly divided into five groups. The results showed that the sheep treated for coccidiosis had considerably decreased average daily gain (ADG) during both administration and withdrawal of the drug compared to the control group. Furthermore, at days 14, 21, 28 and 35, respectively, the three herbs and diclazuril had similar anticoccidial effects, with lower oocysts per gram (OPG) than the control group. On day 78, OPG in the three herbal groups was significantly lower than in the diclazuril group. In addition, the abundance and composition of the gut microbiota were changed in sheep treated with the three herbs and diclazuril compared to the untreated sheep. Moreover, some intestinal microorganisms have a correlation with OPG and ADG when using Spearman correlation analysis. In summary, our results suggest that all three herbs produce anticoccidial effects similar to diclazuril and modulate the balance of gut microbiota in growing lambs.

Keywords: Epizootiology, microbiome, Eimeria, prevention and treatment, sheep

Received: June 28, 2023; Revised: January 24, 2024; Accepted: February 5, 2024; Published online: April 17, 2024  Show citation

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He, Y., Wang, Z., Li, S., Chen, P., Liu, K., Li, M., ... Jian, F. (2024). Effects of three kinds of Chinese herbs on growth performance, oocysts output and gut microbiota in growing lambs with coccidiosis. Folia Parasitologica71, Article 2024.009. https://doi.org/10.14411/fp.2024.009
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References

  1. Abad P., Arroyo-Manzanares N., Ariza J.J., Baños A., García-Campaña A.M. 2020: Effect of Allium extract supplementation on egg quality, productivity, and intestinal microbiota of laying hens. Animals (Basel) 11: 41. Go to original source... Go to PubMed...
  2. Alfwuaires M.A., Algefare A.I., Afkar E., Salam S.A., El-Moaty H.I.A., Badr G.M. 2021: Immunomodulatory assessment of Portulaca oleracea L. extract in a mouse model of colitis. Biomed. Pharmacother. 143: 112148. Go to original source... Go to PubMed...
  3. Bangoura B., Bardsley K.D. 2020: Ruminant coccidiosis. Vet. Clin. North. Am. Food. Anim. Pract. 36: 187-203. Go to original source... Go to PubMed...
  4. Bangoura B., Bhuiya M.A.I., Kilpatrick M. 2022: Eimeria infections in domestic and wild ruminants with reference to control options in domestic ruminants. Parasitol. Res. 121: 2207-2232. Go to original source... Go to PubMed...
  5. Bao M., Hou K., Xin C., Zeng D., Cheng C., Zhao H., Wang Z., Wang L. 2022: Portulaca oleracea L. extract alleviated Type 2 Diabetes via modulating the gut microbiota and serum branched-chain amino acid metabolism. Mol. Nutr. Food Res. 66: e2101030. Go to original source... Go to PubMed...
  6. Bauer B.U., Pomroy W.E., Gueydon J., Gannac S., Scott I., Pfister K. 2010: Comparison of the FLOTAC technique with the McMaster method and the Baermann technique to determine counts of Dictyocaulus eckerti L1 and strongylid eggs in faeces of red deer (Cervus elaphus). Parasitol. Res. 107: 555-560. Go to original source... Go to PubMed...
  7. Borlinghaus J., Albrecht F., Gruhlke M.C., Nwachukwu I.D., Slusarenko A.J. 2014: Allicin: chemistry and biological properties. Molecules 19: 12591-12618. Go to original source... Go to PubMed...
  8. Chang J.S., Chiang L.C., Chen C.C., Liu L.T., Wang K.C., Lin C.C. 2001: Antileukemic activity of Bidens pilosa L. var. minor (Blume) Sherff and Houttuynia cordata Thunb. Am. J. Chin. 29: 303-312. Go to original source... Go to PubMed...
  9. Chen M.Y., Li H., Lu X.X., Ling L.J., Weng H.B., Sun W., Chen D.F., Zhang Y.Y. 2019: Houttuynia cordata polysaccharide alleviated intestinal injury and modulated intestinal microbiota in H1N1 virus infected mice. Chin. J. Nat. Med. 17: 187-197. Go to original source... Go to PubMed...
  10. Christaki E., Marcou M., Tofarides A. 2020: Antimicrobial resistance in bacteria: mechanisms, evolution, and persistence. J. Mol. Evol. 88: 26-40. Go to original source... Go to PubMed...
  11. De Greef D., Barton E. M., Sandberg E. N., Croley C. R., Pumarol J., Wong T. L., Das N., Bishayee A. 2021: Anticancer potential of garlic and its bioactive constituents: a systematic and comprehensive review. Semin. Cancer Biol. 73: 219-264. Go to original source... Go to PubMed...
  12. Diao N.C., Zhao B., Chen Y., Wang Q., Chen Z.Y., Yang Y., Sun Y. H., Shi J.F., Li J.M., Shi K., Gong Q.L., Du R. 2022: Prevalence of Eimeria spp. among goats in China: a systematic review and meta-analysis. Front. Cell Infect. Microbiol. 12: 806085. Go to original source... Go to PubMed...
  13. Dkhil M.A., Abdel-Baki A.S., Wunderlich F., Sies H., Al-Quraishy S. 2011: Anticoccidial and antiinflammatory activity of garlic in murine Eimeria papillata infections. Vet. Parasitol. 175: 66-72. Go to original source... Go to PubMed...
  14. Du S., Li H., Cui Y., Yang L., Wu J., Huang H., Chen Y., Huang W., Zhang R., Yang J., Chen D., Li Y., Zhang S., Zhou J., Wei Z., Chow N.T. 2012: Houttuynia cordata inhibits lipopolysaccharide-induced rapid pulmonary fibrosis by up-regulating IFN-gamma and inhibiting the TGF-beta1/Smad pathway. Int. Immunopharmacol. 13: 331-340. Go to original source... Go to PubMed...
  15. El-Saber Batiha G., Magdy Beshbishy A., Wasef L.G., Elewa Y.H.A., Al-Sagan A.A., Abd El-Hack M.E., Taha A.E., Abd-Elhakim Y.M., Prasad Devkota H. 2020: Chemical constituents and pharmacological activities of garlic (Allium sativum L.): a review. Nutrients 12: 872. Go to original source... Go to PubMed...
  16. Fu Q., Zhou S., Yu M., Lu Y., He G., Huang X., Huang Y. 2022: Portulaca oleracea polysaccharides modulate intestinal microflora in aged rats. Front. Microbiol. 13: 841397. Go to original source... Go to PubMed...
  17. Karimi G., Hosseinzadeh H., Ettehad N. 2004: Evaluation of the gastric antiulcerogenic effects of Portulaca oleracea L. extracts in mice. Phytother. Res. 18: 484-487. Go to original source... Go to PubMed...
  18. Kumar A., Sreedharan S., Kashyap A. K., Singh P., Ramchiary N. 2021: A review on bioactive phytochemicals and ethnopharmacological potential of purslane (Portulaca oleracea L.). Heliyon 8: e08669. Go to original source... Go to PubMed...
  19. Kumar M., Prasad S.K., Krishnamurthy S., Hemalatha S. 2014: Antihyperglycemic activity of Houttuynia cordata Thunb. in Streptozotocin-induced diabetic rats. Adv. Pharmacol. Sci. 2014: 809438. Go to original source... Go to PubMed...
  20. Kwon T.K., Kim J.C. 2014: In vitro skin permeation and anti-atopic efficacy of lipid nanocarriers containing water soluble extracts of Houttuynia cordata. Drug Dev. Ind. Pharm. 40: 1350-1357. Go to original source... Go to PubMed...
  21. Lee G., You H.J., Bajaj J.S., Joo S.K., Yu J., Park S., Kang H., Park J.H., Kim J.H., Lee D.H., Lee S., Kim W., Ko G. 2020: Distinct signatures of gut microbiome and metabolites associated with significant fibrosis in non-obese NAFLD. Nat. Commun. 11: 4982. Go to original source... Go to PubMed...
  22. Macrelli M.D.L., Mitchell S. 2019: Coccidiosis in sheep. Vet. Rec. 184: 549-550. Go to original source... Go to PubMed...
  23. Magry¶ A., Olender A., Tchórzewska D. 2021: Antibacterial properties of Allium sativum L. against the most emerging multidrug-resistant bacteria and its synergy with antibiotics. Arch. Microbiol. 203: 2257-2268. Go to original source... Go to PubMed...
  24. Mohamaden W. I., Sallam N. H., Abouelhassan E. M. 2018: Prevalence of Eimeria species among sheep and goats in Suez Governorate, Egypt. Int. J. Vet. Sci. Med. 6: 65-72. Go to original source... Go to PubMed...
  25. Nweze N. E., Obiwulu I. S. 2009: Anticoccidial effects of Ageratum conyzoides. J. Ethnopharmacol. 122: 6-9. Go to original source... Go to PubMed...
  26. Palaniswamy U. R., McAvoy R. J., Bible B. B. 2001: Stage of harvest and polyunsaturated essential fatty acid concentrations in purslane (Portulaca oleraceae) leaves. J. Agric. Food Chem. 49: 3490-3493. Go to original source... Go to PubMed...
  27. Panyod S., Wu W.K., Lu K.H., Liu C.T., Chu Y.L., Ho C.T., Hsiao W.W., Lai Y.S., Chen W.C., Lin Y.E., Lin S.H., Wu M.S., Sheen L.Y. 2020: Allicin modifies the composition and function of the gut microbiota in alcoholic hepatic steatosis mice. J. Agric. Food Chem. 68: 3088-3098. Go to original source... Go to PubMed...
  28. Parker B.J., Wearsch P.A., Veloo A.C.M., Rodriguez-Palacios A. 2020: The genus Alistipes: gut bacteria with emerging implications to inflammation, cancer, and mental health. Front. Immunol. 11: 906. Go to original source... Go to PubMed...
  29. Quiroz-Castañeda R.E., Dantán-González E. 2015: Control of avian coccidiosis: future and present natural alternatives. BioMed Res. Int. 2015: 430610. Go to original source... Go to PubMed...
  30. Rafiq S., Hao H., Ijaz M., Raza A. 2022: Pharmacological effects of Houttuynia cordata Thunb (H. cordata): a comprehensive review. Pharmaceuticals (Basel). 15: 1079. Go to original source... Go to PubMed...
  31. Rahimi V.B., Ajam F., Rakhshandeh H., Askari V.R. 2019: A pharmacological review on Portulaca oleracea L.: focusing on anti-inflammatory, anti-oxidant, immuno-modulatory and antitumor activities. J Pharmacopuncture 22: 7-15. Go to original source... Go to PubMed...
  32. Shingnaisui K., Dey T., Manna P., Kalita J. 2018: Therapeutic potentials of Houttuynia cordata Thunb. against inflammation and oxidative stress: a review. J. Ethnopharmacol. 220: 35-43. Go to original source... Go to PubMed...
  33. Tavella T., Rampelli S., Guidarelli G., Bazzocchi A., Gasperini C., Pujos-Guillot E., Comte B., Barone M., Biagi E., Candela M., Nicoletti C., Kadi F., Battista G., Salvioli S., O'Toole P.W., Franceschi C., Brigidi P., Turroni S., Santoro A. 2021: Elevated gut microbiome abundance of Christensenellaceae, Porphyromonadaceae and Rikenellaceae is associated with reduced visceral adipose tissue and healthier metabolic profile in Italian elderly. Gut Microbes 13: 1-19. Go to original source... Go to PubMed...
  34. Taylor M.A., Catchpole J. 1994: Review article: coccidiosis of domestic ruminants. Appl. Parasitol. 35: 73-86.
  35. Verma T., Aggarwal A., Dey P., Chauhan A.K., Rashid S., Chen K.T., Sharma R. 2023: Medicinal and therapeutic properties of garlic, garlic essential oil, and garlic-based snack food: an updated review. Front. Nutr. 10: 1120377. Go to original source... Go to PubMed...
  36. Waters J.L., Ley R.E. 2019: The human gut bacteria Christensenellaceae are widespread, heritable, and associated with health. BMC Biol. 17: 83. Go to original source... Go to PubMed...
  37. Whitty C.J.M. 2019. Antimicrobial resistance: learning lessons from antiparasitic, antibacterial and antimycobacterial drug resistance in low-income settings. Trans. R. Soc. Trop. Med. Hyg. 113: 105-107. Go to original source... Go to PubMed...
  38. Wu Z., Deng X., Hu Q., Xiao X., Jiang J., Ma X., Wu M. 2021: Houttuynia cordata Thunb: an ethnopharmacological review. Front. Pharmacol. 12: 714694. Go to original source... Go to PubMed...
  39. Zafar H., Saier M.H., Jr. 2021: Gut Bacteroides species in health and disease. Gut Microbes 13: 1-20. Go to original source... Go to PubMed...
  40. Zhang Y., Liu X., Ruan J., Zhuang X., Zhang X., Li Z. 2020: Phytochemicals of garlic: promising candidates for cancer therapy. Biomed. Pharmacother. 123: 109730. Go to original source... Go to PubMed...
  41. Zhou Y.X., Xin H.L., Rahman K., Wang S.J., Peng C., Zhang H. 2015: Portulaca oleracea L.: a review of phytochemistry and pharmacological effects. Biomed. Res. Int. 2015: 925631. Go to original source... Go to PubMed...