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Effect of a multi-strains yeast fractions product plus anticoccidial drug on performance, anticoccidial index, intestinal health, and bone mineralization of broiler chickens infected with Eimeria spp

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Abstract

The aim of this study was to investigate the combined effect of dietary supplementation of a multi-strains yeast fractions product (MSYF) and an anticoccidial on the performance and health of broiler chickens orally challenged with Eimeria spp. oocysts. A total of 192 male, 1-day-old, Ross-308 chicks were randomly allocated into 4 groups with 6 replicates of 8 chicks each, housed in separate cages. All groups were offered ad libitum water and the same basal diets of meal feed. The first group (negative control, NC) was unchallenged, whereas the second group (positive control, PC) was orally challenged with Eimeria spp. oocysts. The other two challenged groups had their diets further supplemented with either a coccidiostat (salinomycin 60 mg/kg feed, SAL) or a combination of a coccidiostat plus the examined MSYF (0.4 g/kg feed) (COMB). The three challenged groups were orally inoculated at 14 days of age with a specific amount of sporulated oocysts, containing 3.5 × 104 Eimeria acervulina, 7.0 × 103 Eimeria maxima, and 5.0 × 103 Eimeria tenella oocysts. Performance parameters were weekly recorded. On day 7 postinfection (p.i), coccidiosis lesions were scored, and intestinal samples were taken for histopathology evaluation as well as for oxidative status analysis. Also, femur and tibia bone mineralization along with their resistance to breaking was assessed. Counts of total aerobes, total anaerobes, coliforms, and lactobacilli were also enumerated in digesta samples from jejunum, ileum, and cecum by conventional microbiological techniques. Samples of intestinal digesta (duodenum, ileum, and ceca) were further subjected to coccidian enumeration by quantitative real-time PCR (qPCR). Fecal oocyst numbers were also determined consecutively on days 17 to 22 and on day 35. All data were subjected to a one-way analysis of variance (ANOVA) or Kruskal–Wallis test, depending on their normality and homoscedasticity. The combination of MSYF plus salinomycin (COMB) when compared to PC had improved (P < 0.05) body weights of chicken up to day 26 of age, as well as higher (P < 0.05) jejunum and cecum lactobacilli counts. Moreover, PC had lower (P < 0.05) duodenum villus height compared to the other three groups and lower (P < 0.05) jejunum villus height compared to NC and the MSYF plus coccidiostat group (COMB). The intestinal lesion scores were higher (P < 0.05) in the PC group, whereas the anticoccidial drug (SAL) and the MSYF plus the COMB tended (P < 0.10) to have less severe macroscopic lesions. The group COMB, when compared to PC, had lower (P < 0.05) oocysts shedding during the acute phase of the challenge (days 17–22). Moreover, the qPCR analysis showed that group COMB had lower (P < 0.05) DNA concentrations for every examined combination of Eimeria spp. and sampling site compared to the PC, but additionally, in some cases, lower (P < 0.05) DNA concentrations compared to group SAL (duodenum E. maxima and E. tenella; ileum E. acervulina, E. maxima, and E. tenella; ceca E. maxima and E. tenella). The combination of MSYF and anticoccidial (COMB) increased bone ash content in both femur and tibia and showed higher values of comprehensive strength. In conclusion, MSYF can be used in combination with salinomycin (COMB) to reduce the negative effects of an Eimeria challenge, as a consequence, improve growth performance in the challenged birds.

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References

  • Allen PC (1997) Production of free radical species during Eimeria maxima infections in chickens. Poult Sci 76:814–821

    Article  CAS  Google Scholar 

  • Allender WJ, Richards TJ (2010) Consumer impact of animal welfare regulation in the California poultry industry. J Agricul Resource Econ 424–442

  • Applegate TJ, Lilburn MS (2002) Growth of the femur and tibia of a commercial broiler line. Poult Sci 81:1289–1294

    Article  CAS  Google Scholar 

  • Aviagen (2019) ROSS Nutrition Specifications Aviagen: Huntsville USA

  • Biggs P, Parsons CM, Fahey GC (2007) The effects of several oligosaccharides on growth performance, nutrient digestibilities, and cecal microbial populations in young chicks. Poult Sci 86:2327–2336

    Article  CAS  Google Scholar 

  • Blake JP, Hess JB, Maklin KS, Bilgili SF, Sefton AE, Kocher A (2006) Mannan oligosaccharide (Bio-Mos®) supplementation of wheat-based diets for broilers. In Proceeding of the EPC 2006–12th European Poultry Conf

  • Blake DP, Tomley FM (2014) Securing poultry production from the ever-present Eimeria challenge. Trends Parasitol 30:12–19

    Article  Google Scholar 

  • Blake DP, Knox J, Dehaeck B, Huntington B, Rathinam T, Ravipati V, Tomley FM (2020) Re-calculating the cost of coccidiosis in chickens. Vet Res 51:1–14

    Article  Google Scholar 

  • Bozkurt M, Giannenas I, Küçükyilmaz K, Christaki E, Florou-Paneri P (2013) An update on approaches to controlling coccidia in poultry using botanical extracts. Br Poult Sci 54:713–727

    Article  CAS  Google Scholar 

  • Bozkurt M, Aysul N, Küçükyilmaz K, Aypak S, Ege G, Catli AU, Çınar M (2014) Efficacy of in-feed preparations of an anticoccidial, multienzyme, prebiotic, probiotic, and herbal essential oil mixture in healthy and Eimeria spp.-infected broilers. Poult Sci 93:389–399

    Article  CAS  Google Scholar 

  • Chapman HD (1998) Evaluation of the efficacy of anticoccidial drugs against Eimeria species in the fowl. International J Parasitol 28:1141–1144

    Article  CAS  Google Scholar 

  • Charan J, Kantharia ND (2013) How to calculate sample size in animal studies. J Pharmacol Pharmacother 4:303–306. https://doi.org/10.4103/0976-500X.119726

    Article  Google Scholar 

  • Cook RH, Bird FH (1973) Duodenal villus area and epithelial cellular migration in conventional and germ-free chicks. Poult Sci 52:2276–2280

    Article  CAS  Google Scholar 

  • Dalloul RA, Lillehoj HS, Shellem TA, Doerr JA (2003) Enhanced mucosal immunity against Eimeria acervulina in broilers fed a Lactobacillus-based probiotic. Poult Sci 82:62–66

    Article  CAS  Google Scholar 

  • Faul F, Erdfelder E, Lang AG, Buchner A (2007) G* Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Resear Methods 39(2):175–191

    Article  Google Scholar 

  • Gao J, Zhang HJ, Yu SH, Wu SG, Yoon I, Quigley J, Qi GH (2008) Effects of yeast culture in broiler diets on performance and immunomodulatory functions. Poultry Sci 87(7):1377–1384

    Article  CAS  Google Scholar 

  • Garcia-Lafuente A, Antolin M, Guarner F, Crespo E, Malagelada JR (2001) Modulation of colonic barrier function by the composition of the commensal flora in the rat. Gut 48:503–507

    Article  CAS  Google Scholar 

  • Gaucher ML, Quessy S, Letellier A, Arsenault J, Boulianne M (2015) Impact of a drug-free program on broiler chicken growth performances, gut health, Clostridium perfringens and Campylobacter jejuni occurrences at the farm level. Poult Sci 94:1791–1801

    Article  CAS  Google Scholar 

  • Gava MS, Moraes LB, Carvalho D, Chitolina GZ, Fallavena LCB, Moraes HLDS, Salle CTP (2015) Determining the best sectioning method and intestinal segment for morphometric analysis in broilers. Brazil J Poult Sci 17:145–149

    Article  Google Scholar 

  • Giannenas I, Florou-Paneri P, Papazahariadou M, Christaki E, Botsoglou NA, Spais AB (2003) Effect of dietary supplementation with oregano essential oil on performance of broilers after experimental infection with Eimeria tenella. Archives Anim Nutr 57:99–106

    Article  CAS  Google Scholar 

  • Giannenas I, Tsalie E, Triantafillou E, Hessenberger S, Teichmann K, Mohnl M, Tontis D (2014) Assessment of probiotics supplementation via feed or water on the growth performance, intestinal morphology and microflora of chickens after experimental infection with Eimeria acervulina, Eimeria maxima and Eimeria tenella. Avian Pathol 43:209–216

    Article  CAS  Google Scholar 

  • Giannenas I, Sidiropoulou E, Bonos E, Christaki E, Florou-Paneri P (2020) The history of herbs, medicinal and aromatic plants, and their extracts: past, current situation and future perspectives. In Feed Additives (pp. 1–18). Academic Press

  • Hessenberger S, Schatzmayr G, Teichmann K (2016) In vitro inhibition of Eimeria tenella sporozoite invasion into host cells by probiotics. Vet Parasitol 229:93–98

    Article  CAS  Google Scholar 

  • Jarquín D, Hugo V (2019) Detection and quantification of house mouse Eimeria at the species level–Challenges and solutions for the assessment of coccidia in wildlife. International J Parasitol Parasites Wildlife 10:29–40

    Article  Google Scholar 

  • Jin LZ, Ho YW, Abdullah N, Jalaludin S (1997) Probiotics in poultry: modes of action. World’s Poult Sci J 53:351–368

    Article  Google Scholar 

  • Johnson J, Reid WM (1970) Anticoccidial drugs: lesion scoring techniques in battery and floor-pen experiments with chickens. Experimental Parasitol 28:30–36

    Article  CAS  Google Scholar 

  • Kasornpikul C, Chaiyasut C, Sirithanyalug B, Aeagwanich W, Pewnim T (2009) Effect of the probiotic Lactobacillus plantalum CMU-FP002 on oocyst shedding by broilers inoculated with Eimeria tenella. Avian Biol Res 2:157–159

    Article  Google Scholar 

  • Knowles TG, Kestin SC, Haslam SM, Brown SN, Green LE, Butterworth A, Nicol CJ (2008) Leg disorders in broiler chickens: prevalence, risk factors and prevention. PLoS ONE 3:e1545

    Article  Google Scholar 

  • Lee SH, Lillehoj HS, Dalloul RA, Park DW, Hong YH, Lin JJ (2007) Influence of Pediococcus-based probiotic on coccidiosis in broiler chickens. Poult Sci 86:63–66

    Article  CAS  Google Scholar 

  • Li C, Niu Z, Zou M, Liu S, Wang M, Gu X, Jha R (2020) Probiotics, prebiotics, and synbiotics regulate the intestinal microbiota differentially and restore the relative abundance of specific gut microorganisms. J Dairy Sci 103(7):5816–5829

    Article  CAS  Google Scholar 

  • Macdonald SE, Nolan MJ, Harman K, Boulton K, Hume DA, Tomley FM, Blake DP (2017) Effects of Eimeria tenella infection on chicken caecal microbiome diversity, exploring variation associated with severity of pathology. PLoS ONE 12:e0184890

    Article  Google Scholar 

  • Miles RD, Butcher GD, Henry PR, Littell RC (2006) Effect of antibiotic growth promoters on broiler performance, intestinal growth parameters, and quantitative morphology. Poult Sci 85:476–485

    Article  CAS  Google Scholar 

  • Mengistu BM, Bitsue HK, Huang K (2021) The effects of selenium-enriched probiotics on growth performance, oocysts shedding, intestinal cecal lesion scores, antioxidant capacity, and mRNA gene expression in chickens infected with Eimeria tenella. Biol Trace Element Res 199:278–291

    Article  Google Scholar 

  • Mookiah S, Sieo CC, Ramasamy K, Abdullah N, Ho YW (2014) Effects of dietary prebiotics, probiotic and synbiotics on performance, caecal bacterial populations and caecal fermentation concentrations of broiler chickens. J Sci Food Agriculture 94(2):341–348

    Article  CAS  Google Scholar 

  • Mountzouris KC, Tsirtsikos P, Kalamara E, Nitsch S, Schatzmayr G, Fegeros K (2007) Evaluation of the efficacy of a probiotic containing Lactobacillus, Bifidobacterium, Enterococcus, and Pediococcus strains in promoting broiler performance and modulating cecal microflora composition and metabolic activities. Poult Sci 86:309–317

    Article  CAS  Google Scholar 

  • O’Flaherty S, Saulnier D, Pot B, Versalovic J (2010) How can probiotics and prebiotics impact mucosal immunity? Gut Microbes 1:293–300

    Article  Google Scholar 

  • Oikeh I, Sakkas P, Taylor J, Giannenas I, Blake DP, Kyriazakis I (2019) Effects of reducing growth rate via diet dilution on bone mineralization, performance and carcass yield of coccidia-infected broilers. Poult Sci 98:5477–5487

    Article  CAS  Google Scholar 

  • Ojimelukwe AE, Emedhem ED, Agu GO, Nduka FO, Abah EA (2018) Populations of Eimeria tenella express resistance to commonly used anticoccidial drugs in southern Nigeria. International J Vet Sci Medic 6:192–200

    Article  Google Scholar 

  • Palamidi I, Mountzouris KC (2018) Diet supplementation with an organic acids-based formulation affects gut microbiota and expression of gut barrier genes in broilers. Anim Nutr 4:367–377

    Article  Google Scholar 

  • Peek HW (2010) Resistance to anticoccidial drugs: alternative strategies to control coccidiosis in broilers. Utrecht University

  • Rawling MD, Pontefract N, Rodiles A, Anagnostara I, Leclercq E, Schiavone M, Merrifield DL (2019) The effect of feeding a novel multistrain yeast fraction on European seabass (Dicentrachus labrax) intestinal health and growth performance. J World Aquaculture Society 50(6):1108–1122

    Article  CAS  Google Scholar 

  • Rehman HU, Vahjen W, Awad WA, Zentek J (2007) Indigenous bacteria and bacterial metabolic products in the gastrointestinal tract of broiler chickens. Archives Anim Nutr 61:319–335

    Article  Google Scholar 

  • Sakkas P, Oikeh I, Blake DP, Nolan MJ, Bailey RA, Oxley A, Kyriazakis I (2018) Does selection for growth rate in broilers affect their resistance and tolerance to Eimeria maxima. Vet Parasitol 258:88–98

    Article  Google Scholar 

  • Schneeman BO (1982) Pancreatic and digestive function. In Dietary fiber in health and disease 73–83 Springer Boston MA

  • Skoufos I, Bonos E, Anastasiou I, Tsinas A, Tzora A (2020) Effects of phytobiotics in healthy or disease challenged animals. Feed Additives 311–337

  • Stier H, Ebbeskotte V, Gruenwald J (2014) Immune-modulatory effects of dietary yeast beta-1, 3/1, 6-D-glucan. Nutrition J 13(1):1–9

    Article  Google Scholar 

  • Sung WE, Haryono M (2017) Quality change after oven-drying and frozen storage of bluesripe herring (Herklotsichthys quadrimaculatus). J Food Nutr Res 5:935–940

    Article  CAS  Google Scholar 

  • Tierney J, Gowing H, Van Sinderen D, Flynn S, Stanley L, McHardy N, Mulcahy G (2004) In vitro inhibition of Eimeria tenella invasion by indigenous chicken Lactobacillus species. Vet Parasitol 122:171–182

    Article  CAS  Google Scholar 

  • Travers MA, Florent I, Kohl L, Grellier P (2011) Probiotics for the control of parasites: an overview. J Parasitol Res Volume 2011, Article ID 610769, 11 pages. https://doi.org/10.1155/2011/610769

  • Tsiouris V, Kontominas MG, Filioussis G, Chalvatzi S, Giannenas I, Papadopoulos G, Georgopoulou I (2020) The effect of whey on performance, gut health and bone morphology parameters in broiler chicks. Foods 9:588

    Article  CAS  Google Scholar 

  • Tzora A, Giannenas I, Karamoutsios A, Papaioannou N, Papanastasiou D, Bonos E, Skoufos S, Bartzanas T, Skoufos I (2017) Effects of oregano, attapulgite, benzoic acid and their blend on chicken performance, intestinal microbiology and intestinal morphology. J Poult Sci 54:218–227

    Article  CAS  Google Scholar 

  • Velkers FC, Blake DP, Graat EAM, Vernooij JCM, Bouma A, De Jong MCM, Stegeman JA (2010) Quantification of Eimeria acervulina in faeces of broilers: comparison of McMaster oocyst counts from 24 h faecal collections and single droppings to real-time PCR from cloacal swabs. Vet Parasitol 169:1–7

    Article  CAS  Google Scholar 

  • Vieira AM, Soratto TAT, Cardinal KM, Wagner G, Hauptli L, Lima ALF et al (2020) Modulation of the intestinal microbiota of broilers supplemented with monensin or functional oils in response to challenge by Eimeria spp. PLoS ONE 15(8):e0237118. https://doi.org/10.1371/journal.pone.0237118

    Article  CAS  Google Scholar 

  • Voidarou C, Vassos D, Kegos T, Koutsotoli A, Tsiotsias A, Skoufos J, Tzora A, Maipa V, Alexopoulos A, Bezirtzoglou E (2007) Aerobic and anaerobic microbiology of the immersion chilling in poultry. Poult Sci 86:1218–1222

    Article  CAS  Google Scholar 

  • Vrba V, Blake DP, Poplstein M (2010) Quantitative real-time PCR assays for detection and quantification of all seven Eimeria species that infect the chicken. Vet Parasitol 174:183–190

    Article  CAS  Google Scholar 

  • Vyncke W (1975) Evaluation of the direct thiobarbituric acid extraction method for determining oxidative rancidity in mackerel (Scomber scombrus L.). Fette Seifen Anstrichmittel 77:239–240

    Article  CAS  Google Scholar 

  • Wang Y, Lv X, Li X, Zhao J, Zhang K, Hao X, Liu H (2021) Protective effect of Lactobacillus Plantarum P8 on the growth performance, intestinal health and microbiota in Eimeria-infected broilers

  • Williams RB (2005) Intercurrent coccidiosis and necrotic enteritis of chickens: rational, integrated disease management by maintenance of gut integrity. Avian Pathol 34:159–180

    Article  CAS  Google Scholar 

  • Wu SB, Stanley D, Rodgers N, Swick RA, Moore RJ (2014) Two necrotic enteritis predisposing factors, dietary fishmeal and Eimeria infection, induce large changes in the caecal microbiota of broiler chickens. Vet Microbiol 169:188–197

    Article  Google Scholar 

  • Yason CV, Summers BA, Schat KA (1987) Pathogenesis of rotavirus infection in various age groups of chickens and turkeys: pathology. American J Vet Resear 48:927–938

    CAS  Google Scholar 

Download references

Funding

This research study was partly funded by Greece and the European Union (European Regional Development Fund) in the context of “Research—Create—Innovate” within the Operational Program (Competitiveness, Entrepreneurship, and Innovation (ΕΠΑΝΕΚ) of the NSRF 2014–2020. Project code: Τ1ΕΔΚ-03856. The acronym “GREEN POULTRY MEAT ANTIFREE.” Also, DANSTAR FERMENT AG is acknowledged for partial funding of this trial under the project code 71736 of the Research Committee of Aristotle University, titled: Effects of dietary supplementation of paraprobiotic on broiler performance and broiler general and intestinal health.

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Authors and Affiliations

  1. Laboratory of Nutrition, School of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece

    Ilias Giannenas, Erasmia Sidiropoulou & Stella Dokou

  2. Unit of Avian Medicine, Clinic of Farm Animals, School of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece

    Vasilios Tsiouris

  3. Laboratory of Animal Science, Nutrition and Biotechnology, Department of Agriculture, School of Agriculture, University of Ioannina, Kostakioi Artas, 47100, Arta, Greece

    Eleftherios Bonos & Ioannis Skoufos

  4. Laboratory of Pathology, School of Veterinary Medicine, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Ioanna Stylianaki

  5. Laboratory of Animal Husbandry, Department of Animal Production, School of Agriculture, Aristotle University of Thessaloniki, 54124, Thessaloniki, Greece

    Zoitsa Basdagianni

  6. Lallemand SAS, 31701, Blagnac, France

    Vanessa Demey

  7. Laboratory of Parasitology and Parasitic Diseases, School of Veterinary Medicine, Aristotle University of Thessaloniki, Thessaloniki, Greece

    Elias Papadopoulos

  8. Laboratory of Animal Health, Department of Agriculture, School of Agriculture, Food Hygiene and Quality, University of Ioannina, Kostakioi Artas, 47100, Arta, Greece

    Athina Tzora

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  1. Ilias Giannenas
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Correspondence to Ilias Giannenas.

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Giannenas, I., Tsiouris, V., Bonos, E. et al. Effect of a multi-strains yeast fractions product plus anticoccidial drug on performance, anticoccidial index, intestinal health, and bone mineralization of broiler chickens infected with Eimeria spp. Comp Clin Pathol 32, 15–28 (2023). https://doi.org/10.1007/s00580-022-03389-3

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