Enhancing gut health and performance of grower-finisher pigs: assessing the efficacy of the mixture of microencapsulated essential oils and saponins

Sung J. Yu; Andrew Morris; Advait Kayal; Thi Thu Hao Van; Dragana Stanley; Yadav S. Bajagai

doi:10.1071/AN23215

RESEARCH ARTICLE (Open Access)

Previous Next Contents Vol 64(1)

Enhancing gut health and performance of grower-finisher pigs: assessing the efficacy of the mixture of microencapsulated essential oils and saponins

Sung J. Yu

^A , Andrew Morris ^B , Advait Kayal

^A , Thi Thu Hao Van

^C , Dragana Stanley

^A and Yadav S. Bajagai

^A ^*

+ Author Affiliations

- Author Affiliations

^A Central Queensland University, Institute for Future Farming Systems, Rockhampton, Qld 4701, Australia.

^B Riverbend Pork Group, 487-489 Ruthven Street, Toowoomba, Qld 4350, Australia.

^C School of Science, RMIT University, Bundoora, Vic. 3083, Australia.

^* Correspondence to: y.sharmabajagai@cqu.edu.au

Handling Editor: Cormac O’Shea

Animal Production Science 64, AN23215 https://doi.org/10.1071/AN23215

Submitted: 7 June 2023 Accepted: 2 November 2023 Published: 24 November 2023

© 2024 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)

Abstract

Context

The livestock industry demands alternative approaches to maintain animal health and productivity without using antimicrobials. Phytogenic feed additives, consisting of plant-derived compounds, offer promising benefits to grower-finisher pigs’ gut microbiota and overall health.

Aims

This study investigated the impact of essential oils and saponins as phytogenic feed additives on the gut microbiota and productivity of grower-finisher pigs.

Methods

Four hundred male Large White × Landrace pigs were randomly allocated into control and treatment groups and provided with a basal diet. The treatment group supplemented commercial phytogenic feed additives. Performance data, general health, cumulative mortality, and bodyweight were monitored. Intestinal samples from different gut locations and rectal swab samples were collected for microbiota analysis.

Key results

No significant difference in weight was observed between the two groups; however, the phytogenic feed additives notably affected gut microbiota. Greater microbial diversity and changes in genera abundance were evident. Campylobacter and Clostridium increased, while beneficial Lactobacillus increased, and Escherichia decreased. The supplemented group demonstrated more consistent growth, with higher minimum weights.

Conclusions

Phytogenic feed additives have a significant impact on the gut microbiota of grower-finisher pigs. A diverse microbial community and specific changes in genera abundance were observed, indicating the potential role of these additives in modulating gut health.

Implications

This study emphasises the potential advantages of using phytogenic feed additives to improve the health and productivity of livestock without the use of antibiotics.

Keywords: essential oils, grower-finisher pigs, gut microbiota, natural antimicrobial product, phytogenic product, post-weaning diarrhoea, saponins, swine, rosemary, thyme.

References

Abdelli N, Sola-Oriol D, Perez JF (2021) Phytogenic feed additives in poultry: achievements, prospective and challenges. Animals 11, 3471.
| Crossref | Google Scholar |

Anderson MJ, Clarke KR, Gorley RN (2008) ‘PERMANOVA+ for PRIMER: guide to software statistical methods.’ (PRIMER-E: Plymouth, UK)

Bajagai YS, Alsemgeest J, Moore RJ, Van TTH, Stanley D (2020) Phytogenic products, used as alternatives to antibiotic growth promoters, modify the intestinal microbiota derived from a range of production systems: an in vitro model. Applied Microbiology and Biotechnology 104, 10631-10640.
| Crossref | Google Scholar | PubMed |

Bajagai YS, Petranyi F, Yu SJ, Lobo E, Batacan R, Jr, Kayal A, Horyanto D, Ren X, Whitton MM, Stanley D (2022) Phytogenic supplement containing menthol, carvacrol and carvone ameliorates gut microbiota and production performance of commercial layers. Scientific Reports 12, 11033.
| Crossref | Google Scholar | PubMed |

Bartos P, Dolan A, Smutny L, Sistkova M, Celjak I, Soch M, Havelka Z (2016) Effects of phytogenic feed additives on growth performance and on ammonia and greenhouse gases emissions in growing-finishing pigs. Animal Feed Science and Technology 212, 143-148.
| Crossref | Google Scholar |

Bauer BW, Gangadoo S, Bajagai YS, Van TTH, Moore RJ, Stanley D (2019) Oregano powder reduces Streptococcus and increases SCFA concentration in a mixed bacterial culture assay. PLoS ONE 14, e0216853.
| Crossref | Google Scholar | PubMed |

Bengtsson B, Wierup M (2006) Antimicrobial resistance in Scandinavia after a ban of antimicrobial growth promoters. Animal Biotechnology 17, 147-156.
| Crossref | Google Scholar | PubMed |

Bhat MA, Mishra AK, Tantray JA, Alatawi HA, Saeed M, Rahman S, Jan AT (2022) Gut microbiota and cardiovascular system: an intricate balance of health and the diseased state. Life 12, 1986.
| Crossref | Google Scholar |

Bolyen E, Rideout JR, Dillon MR, Bokulich NA, Abnet CC, Al-Ghalith GA, Alexander H, Alm EJ, Arumugam M, Asnicar F, Bai Y, Bisanz JE, Bittinger K, Brejnrod A, Brislawn CJ, Brown CT, Callahan BJ, Caraballo-Rodriguez AM, Chase J, Cope EK, Da Silva R, Diener C, Dorrestein PC, Douglas GM, Durall DM, Duvallet C, Edwardson CF, Ernst M, Estaki M, Fouquier J, Gauglitz JM, Gibbons SM, Gibson DL, Gonzalez A, Gorlick K, Guo J, Hillmann B, Holmes S, Holste H, Huttenhower C, Huttley GA, Janssen S, Jarmusch AK, Jiang L, Kaehler BD, Kang KB, Keefe CR, Keim P, Kelley ST, Knights D, Koester I, Kosciolek T, Kreps J, Langille MGI, Lee J, Ley R, Liu Y-X, Loftfield E, Lozupone C, Maher M, Marotz C, Martin BD, McDonald D, McIver LJ, Melnik AV, Metcalf JL, Morgan SC, Morton JT, Naimey AT, Navas-Molina JA, Nothias LF, Orchanian SB, Pearson T, Peoples SL, Petras D, Preuss ML, Pruesse E, Rasmussen LB, Rivers A, Robeson MS, 2nd, Rosenthal P, Segata N, Shaffer M, Shiffer A, Sinha R, Song SJ, Spear JR, Swafford AD, Thompson LR, Torres PJ, Trinh P, Tripathi A, Turnbaugh PJ, Ul-Hasan S, van der Hooft JJJ, Vargas F, Vazquez-Baeza Y, Vogtmann E, von Hippel M, Walters W, et al. (2019) Reproducible, interactive, scalable and extensible microbiome data science using QIIME 2. Nature Biotechnology 37, 852-857.
| Crossref | Google Scholar | PubMed |

Callahan BJ, McMurdie PJ, Rosen MJ, Han AW, Johnson AJA, Holmes SP (2016) DADA2: high-resolution sample inference from Illumina amplicon data. Nature Methods 13, 581-583.
| Crossref | Google Scholar | PubMed |

Carrique-Mas JJ, Bryant JE, Cuong NV, Hoang NVM, Campbell J, Hoang NV, Dung TTN, Duy DT, Hoa NT, Thompson C, Hien VV, Phat VV, Farrar J, Baker S (2014) An epidemiological investigation of Campylobacter in pig and poultry farms in the Mekong delta of Vietnam. Epidemiology and Infection 142, 1425-1436.
| Crossref | Google Scholar | PubMed |

Chen X, Xu J, Ren E, Su Y, Zhu W (2018) Co-occurrence of early gut colonization in neonatal piglets with microbiota in the maternal and surrounding delivery environments. Anaerobe 49, 30-40.
| Crossref | Google Scholar | PubMed |

Crisol-Martinez E, Stanley D, Geier MS, Hughes RJ, Moore RJ (2017) Understanding the mechanisms of zinc bacitracin and avilamycin on animal production: linking gut microbiota and growth performance in chickens. Applied Microbiology and Biotechnology 101, 4547-4559.
| Crossref | Google Scholar | PubMed |

Dang DX, Kim IH (2020) Effects of dietary supplementation of Quillaja saponin on growth performance, nutrient digestibility, fecal gas emissions, and meat quality in finishing pigs. Journal of Applied Animal Research 48, 397-401.
| Crossref | Google Scholar |

de Aguiar FC, Solarte AL, Tarradas C, Luque I, Maldonado A, Galan-Relano A, Huerta B (2018) Antimicrobial activity of selected essential oils against Streptococcus suis isolated from pigs. MicrobiologyOpen 7, e00613.
| Crossref | Google Scholar | PubMed |

Denis M, Henrique E, Chidaine B, Tircot A, Bougeard S, Fravalo P (2011) Campylobacter from sows in farrow-to-finish pig farms: risk indicators and genetic diversity. Veterinary Microbiology 154, 163-170.
| Crossref | Google Scholar | PubMed |

Dixon P (2003) Vegan, a package of R functions for community ecology. Journal of Vegetation Science 14, 927-930.
| Crossref | Google Scholar |

Fadrosh DW, Ma B, Gajer P, Sengamalay N, Ott S, Brotman RM, Ravel J (2014) An improved dual-indexing approach for multiplexed 16S rRNA gene sequencing on the Illumina MiSeq platform. Microbiome 2, 6.
| Crossref | Google Scholar | PubMed |

Ghasemi G, Alirezalu A, Ghosta Y, Jarrahi A, Safavi SA, Abbas-Mohammadi M, Barba FJ, Munekata PES, Dominguez R, Lorenzo JM (2020) Composition, antifungal, phytotoxic, and insecticidal activities of thymus kotschyanus essential oil. Molecules 25, 1152.
| Crossref | Google Scholar |

Hou C, Zeng X, Yang F, Liu H, Qiao S (2015) Study and use of the probiotic Lactobacillus reuteri in pigs: a review. Journal of Animal Science and Biotechnology 6, 14.
| Crossref | Google Scholar | PubMed |

Kabat AM, Srinivasan N, Maloy KJ (2014) Modulation of immune development and function by intestinal microbiota. Trends in Immunology 35, 507-517.
| Crossref | Google Scholar | PubMed |

Karaskova K, Suchy P, Strakova E (2015) Current use of phytogenic feed additives in animal nutrition: a review. Czech Journal of Animal Science 60, 521-530.
| Crossref | Google Scholar |

Kim SW, Holanda DM, Gao X, Park I, Yiannikouris A (2019) Efficacy of a yeast cell wall extract to mitigate the effect of naturally co-occurring mycotoxins contaminating feed ingredients fed to young pigs: impact on gut health, microbiome, and growth. Toxins 11, 633.
| Crossref | Google Scholar |

Konstantinov SR, Awati AA, Williams BA, Miller BG, Jones P, Stokes CR, Akkermans ADL, Smidt H, De Vos WM (2006) Post-natal development of the porcine microbiota composition and activities. Environmental Microbiology 8, 1191-1199.
| Crossref | Google Scholar | PubMed |

Lalles J-P, Boudry G, Favier C, Le Floc’h N, Luron I, Montagne L, Oswald IP, Pie S, Piel C, Seve B (2004) Gut function and dysfunction in young pigs: physiology. Animal Research 53, 301-316.
| Crossref | Google Scholar |

Lecerf JM (2020) Is Prevotella/Bacteroides ratio associated with weight loss. Correspondances En Metabolismes Hormones Diabetes Et Nutrition 24, 182.
| Google Scholar |

Lee YK, Mazmanian SK (2010) Has the microbiota played a critical role in the evolution of the adaptive immune system? Science 330, 1768-1773.
| Crossref | Google Scholar | PubMed |

Liu C, Cui Y, Li X, Yao M (2021) microeco: an R package for data mining in microbial community ecology. FEMS Microbiology Ecology 97, fiaa255.
| Crossref | Google Scholar |

Martin M (2011) Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet.Journal 17, 10-12.
| Crossref | Google Scholar |

Mathlouthi N, Bouzaienne T, Oueslati I, Recoquillay F, Hamdi M, Urdaci M, Bergaoui R (2012) Use of rosemary, oregano, and a commercial blend of essential oils in broiler chickens: in vitro antimicrobial activities and effects on growth performance. Journal of Animal Science 90, 813-823.
| Crossref | Google Scholar | PubMed |

Mcmurdie PJ, Holmes S (2013) Phyloseq: an R package for reproducible interactive analysis and graphics of microbiome census data. PLoS ONE 8, e61217.
| Crossref | Google Scholar |

O’Neill J (2016) Tackling drug-resistant infections globally: final report and recommendations. Government of the United Kingdom.

Posthaus H, Kittl S, Tarek B, Bruggisser J (2020) Clostridium perfringens type C necrotic enteritis in pigs: diagnosis, pathogenesis, and prevention. Journal of Veterinary Diagnostic Investigation 32, 203-212.
| Crossref | Google Scholar | PubMed |

Quast C, Pruesse E, Yilmaz P, Gerken J, Schweer T, Yarza P, Peplies J, Glockner FO (2013) The SILVA ribosomal RNA gene database project: improved data processing and web-based tools. Nucleic Acids Research 41, D590-D596.
| Crossref | Google Scholar | PubMed |

Sharma G, Garg N, Hasan S, Shirodkar S (2022) Prevotella: an insight into its characteristics and associated virulence factors. Microbial Pathogenesis 169, 105673.
| Crossref | Google Scholar |

Shehata AA, Yalcin S, Latorre JD, Basiouni S, Attia YA, Abd El-Wahab A, Visscher C, El-Seedi HR, Huber C, Hafez HM, Eisenreich W, Tellez-Isaias G (2022) Probiotics, prebiotics, and phytogenic substances for optimizing gut health in poultry. Microorganisms 10, 395.
| Crossref | Google Scholar |

Shen YB, Voilque G, Odle J, Kim SW (2012) Dietary L-tryptophan supplementation with reduced large neutral amino acids enhances feed efficiency and decreases stress hormone secretion in nursery pigs under social-mixing stress. The Journal of Nutrition 142, 1540-1546.
| Crossref | Google Scholar | PubMed |

Sidiropoulou E, Marugan-Hernandez V, Skoufos I, Giannenas I, Bonos E, Aguiar-Martins K, Lazari D, Papagrigoriou T, Fotou K, Grigoriadou K, Blake DP, Tzora A (2022) In vitro antioxidant, antimicrobial, anticoccidial, and anti-inflammatory study of essential oils of oregano, thyme, and sage from Epirus, Greece. Life 12, 1783.
| Crossref | Google Scholar |

Sinclair A, Xie X, Saab L, Dendukuri N (2016) Lactobacillus probiotics in the prevention of diarrhea associated with Clostridium difficile: a systematic review and Bayesian hierarchical meta-analysis. CMAJ Open 4, E706-E718.
| Crossref | Google Scholar | PubMed |

Smith S (2019) phylosmith: an R-package for reproducible and efficient microbiome analysis with phyloseq-objects. Journal of Open Source Software 4, 1442.
| Crossref | Google Scholar |

Tamanai-Shacoori Z, Smida I, Bousarghin L, Loreal O, Meuric V, Fong SB, Bonnaure-Mallet M, Jolivet-Gougeon A (2017) Roseburia spp.: a marker of health? Future Microbiology 12, 157-170.
| Crossref | Google Scholar | PubMed |

The Lancet (2022) Antimicrobial resistance: time to repurpose the Global Fund. The Lancet 399, 335.
| Crossref | Google Scholar |

Varel VH (2002) Carvacrol and thymol reduce swine waste odor and pathogens: stability of oils. Current Microbiology 44, 38-43.
| Crossref | Google Scholar | PubMed |

Verschuren LMG, Calus MPL, Jansman AJM, Bergsma R, Knol EF, Gilbert H, Zemb O (2018) Fecal microbial composition associated with variation in feed efficiency in pigs depends on diet and sex. Journal of Animal Science 96, 1405-1418.
| Crossref | Google Scholar | PubMed |

Xu CL, Peng K, She Y, Fu F, Shi Q, Lin Y, Xu CB (2023) Preparation of novel trivalent vaccine against enterotoxigenic Escherichia coli for preventing newborn piglet diarrhea. American Journal of Veterinary Research 84, ajvr.22.10.0183.
| Crossref | Google Scholar |

Yu Z, Morrison M (2004) Improved extraction of PCR-quality community DNA from digesta and fecal samples. BioTechniques 36, 808-812.
| Crossref | Google Scholar | PubMed |

Yu SJ, Bajagai YS, Petranyi F, de las Heras-Saldana S, Van TTH, Stanley D (2022) Phytogenic blend improves intestinal health and reduces obesity, diabetes, cholesterol and cancers: a path toward customised supplementation. Antibiotics 11, 1428.
| Crossref | Google Scholar |