Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Animal Production Science Animal Production Science Society
Food, fibre and pharmaceuticals from animals
RESEARCH ARTICLE (Open Access)

Effect of dietary supplementation with essential oils and a Bacillus probiotic on growth performance, diarrhoea and blood metabolites in weaned pigs

B. F. Tan A , T. Lim A and W. Boontiam https://orcid.org/0000-0001-7040-2548 B C D
+ Author Affiliations
- Author Affiliations

A Kemin Industries (Asia) Pte. Limited, 12 Senoko Drive, 758200, Singapore.

B Faculty of Agriculture, Department of Animal Science, Khon Kaen University, Khon Kaen, 40002, Thailand.

C Faculty of Agricultural Technology, Department of Animal Production Technology,King Mongkut’s Institute of Technology Ladkrabang, Bangkok, 10520, Thailand.

D Corresponding author. Email: waewbo@kku.ac.th

Animal Production Science 61(1) 64-71 https://doi.org/10.1071/AN18752
Submitted: 17 December 2018  Accepted: 9 August 2020   Published: 10 September 2020

Journal Compilation © CSIRO 2021 Open Access CC BY-NC-ND

Abstract

Context: Dietary supplementation of essential oils or in combination with a Bacillus probiotic was investigated as an antibiotic growth promoter for weaned pigs.

Aims: To evaluate the effect of essential oils (i.e. thymol and carvacrol mixture) or in combination with a probiotic strain (i.e. Bacillus subtilis PB6) on the growth performance, diarrhoea incidence, ammonia emission and serological profiles of weaned pigs.

Methods: A total of 96 crossbred ([Yorkshire × Landrace] × Duroc) weaned pigs were randomly allotted to one of six treatments based on sex and initial bodyweight. Each group was distributed into four replicates with four pigs each according to a randomised complete block design. The treatments were: (i) positive control, basal diet supplemented with colistin 150 g/tonne and amoxicillin 200 g/tonne; (ii) negative control, basal diet without supplementation; (iii) T3, basal diet supplemented with essential oils 300 g/tonne; (iv) T4, basal diet supplemented with essential oils 600 g/tonne; (v) T5, basal diet supplemented with essential oils 1000 g/tonne; and (vi) T6, basal diet supplemented with essential oils 300 g/tonne diet and Bacillus probiotics 1000 g/tonne.

Key results: The piglets fed with supplements had a significantly higher average daily gain and lower incidence of diarrhoea than the piglets in the negative control (P = 0.001). Feeding the essential oils alone or in combination with probiotics significantly reduced faecal ammonia emission (P = 0.027) and blood urea nitrogen (P = 0.039), while markedly increasing the serum immunoglobulin G concentration of weaned pigs compared with the negative control treatment (P = 0.014). The difference in time of blood collection had significant effects on blood urea nitrogen and immunoglobulins (P = 0.001). However, no significant differences emerged in average daily feed intake, gain : feed ratio, feed efficiency and antibody against swine fever among the treatments.

Conclusions: Diet supplementation with essential oils or in combination with probiotics improved growth performance and immunity, and lowered ammonia emissions and diarrhoea incidence of weaned pigs.

Implications: These findings provide a basis for the application of phytogenic compounds and probiotics as antibiotic growth promoter alternatives in post-weaning diets for pigs.

Additional keywords: classical swine fever virus, gas emission, immunity.


References

Ahmed ST, Hossain ME, Kim GM, Hwang JA, Ji H, Yang CJ (2013) Effects of resveratrol and essential oils on growth performance, immunity, digestibility and fecal microbial shedding in challenged piglets. Asian-Australasian Journal of Animal Sciences 26, 683–690.
Effects of resveratrol and essential oils on growth performance, immunity, digestibility and fecal microbial shedding in challenged piglets.Crossref | GoogleScholarGoogle Scholar | 25049839PubMed |

Amezcua R, Friendship RM, Dewey CE, Gyles C, Fairbrother JM (2002) Presentation of postweaning Escherichia coli diarrhea in southern Ontario, prevalence of hemolytic E. coli serogroups involved, and their antimicrobial resistance patterns. Canadian Journal of Veterinary Research 66, 73–78.

Brown K, Uwiera RRE, Kalmokoff ML, Brooks SPJ, Inglis GD (2017) Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives. International Journal of Antimicrobial Agents 49, 12–24.
Antimicrobial growth promoter use in livestock: a requirement to understand their modes of action to develop effective alternatives.Crossref | GoogleScholarGoogle Scholar | 27717740PubMed |

Cai L, Indrakumar S, Kiarie E, Kim IH (2015) Effects of a multi-strain Bacillus species–based direct-fed microbial on growth performance, nutrient digestibility, blood profile, and gut health in nursery pigs fed corn–soybean meal–based diets. Journal of Animal Science 93, 4336–4342.
Effects of a multi-strain Bacillus species–based direct-fed microbial on growth performance, nutrient digestibility, blood profile, and gut health in nursery pigs fed corn–soybean meal–based diets.Crossref | GoogleScholarGoogle Scholar | 26440333PubMed |

Chen YJ, Min BJ, Cho JH, Kwon OS, Son KS, Kim HJ, Kim IH (2006) Effects of dietary Bacillus-based probiotic on growth performance, nutrients digestibility, blood characteristics and fecal noxious gas content in finishing pigs. Asian-Australasian Journal of Animal Sciences 19, 587–592.
Effects of dietary Bacillus-based probiotic on growth performance, nutrients digestibility, blood characteristics and fecal noxious gas content in finishing pigs.Crossref | GoogleScholarGoogle Scholar |

Cho JH, Chen YJ, Min BJ, Kim HJ, Kwon OS, Shon KS, Kim IH, Kim SJ, Asamer A (2006) Effects of essential oils supplementation on growth performance, IgG concentration and fecal noxious gas concentration of weaned pigs. Asian-Australasian Journal of Animal Sciences 19, 80–85.
Effects of essential oils supplementation on growth performance, IgG concentration and fecal noxious gas concentration of weaned pigs.Crossref | GoogleScholarGoogle Scholar |

Cho JH, Chen YJ, Min BJ, Yoo JS, Wang Y, Kim IH (2008) Effects of reducing dietary crude protein on growth performance, odor gas emission from manure and blood urea nitrogen and IGF-1 concentrations of serum in nursery pigs. Animal Science Journal 79, 453–459.
Effects of reducing dietary crude protein on growth performance, odor gas emission from manure and blood urea nitrogen and IGF-1 concentrations of serum in nursery pigs.Crossref | GoogleScholarGoogle Scholar |

Davis ME, Parrott T, Brown DC, de Rodas BZ, Johnson ZB, Maxwell CV, Rehberger T (2008) Effect of a Bacillus-based direct-fed microbial feed supplement on growth performance and pen cleaning characteristics of growing-finishing pigs. Animal Science Journal 86, 1459–1467.
Effect of a Bacillus-based direct-fed microbial feed supplement on growth performance and pen cleaning characteristics of growing-finishing pigs.Crossref | GoogleScholarGoogle Scholar |

Economou V, Gousia P (2015) Agriculture and food animals as a source of antimicrobial-resistant bacteria. Infection and Drug Resistance 8, 49–61.
Agriculture and food animals as a source of antimicrobial-resistant bacteria.Crossref | GoogleScholarGoogle Scholar | 25878509PubMed |

European Medicines Agency (2016) European Medicines Agency to review guidance on colistin use in animals. Veterinary Record 178, 55.1–55.
European Medicines Agency to review guidance on colistin use in animals.Crossref | GoogleScholarGoogle Scholar |

Fairbrother JM, Nadeau E, Gyles CL (2005) Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies. Animal Health Research Reviews 6, 17–39.
Escherichia coli in postweaning diarrhea in pigs: an update on bacterial types, pathogenesis, and prevention strategies.Crossref | GoogleScholarGoogle Scholar | 16164007PubMed |

Gahan DA, Lynch MB, Callan JJ, O’Sullivan JT, O’Doherty JV (2009) Performance of weanling piglets offered low-, medium- or high-lactose diets supplemented with a seaweed extract from Laminaria spp. Animal 3, 24–31.
Performance of weanling piglets offered low-, medium- or high-lactose diets supplemented with a seaweed extract from Laminaria spp.Crossref | GoogleScholarGoogle Scholar | 22444169PubMed |

Giang HH, Viet TQ, Ogle B, Lindberg JE (2012) Growth performance, digestibility, gut environment and health status in weaned piglets fed a diet supplemented with a complex of lactic acid bacteria alone or in combination with Bacillus subtilis and Saccharomyces boulardii. Livestock Science 143, 132–141.
Growth performance, digestibility, gut environment and health status in weaned piglets fed a diet supplemented with a complex of lactic acid bacteria alone or in combination with Bacillus subtilis and Saccharomyces boulardii.Crossref | GoogleScholarGoogle Scholar |

Hedegaard CJ, Strube ML, Hansen MB, Lindved BK, Lihme A, Boye M, Heegaard PMH (2016) Natural pig plasma immunoglobulins have anti-bacterial effects: potential for use as feed supplement for treatment of intestinal infections in pigs. PLoS One 11, e0147373
Natural pig plasma immunoglobulins have anti-bacterial effects: potential for use as feed supplement for treatment of intestinal infections in pigs.Crossref | GoogleScholarGoogle Scholar | 26824607PubMed |

Hermes RG, Molist F, Ywazaki M, Nofrarías M, Gomez J, Gasa J (2009) Effect of dietary level of protein and fiber on the productive performance and health status of piglets. Journal of Animal Science 87, 3569–3577.
Effect of dietary level of protein and fiber on the productive performance and health status of piglets.Crossref | GoogleScholarGoogle Scholar | 19648494PubMed |

Hong JW, Kim IH, Kwon OS, Min BJ, Lee WB, Shon KS (2004) Influences of plant extract supplementation on performance and blood characteristics in weaned pigs. Asian-Australasian Journal of Animal Sciences 17, 374–378.
Influences of plant extract supplementation on performance and blood characteristics in weaned pigs.Crossref | GoogleScholarGoogle Scholar |

Jiang XR, Agazzi A, Awati A, Vitari F, Bento H, Ferrari A, Alborali GL, Crestani M, Domeneghini C, Bontempo V (2015) Influence of a blend of essential oils and an enzyme combination on growth performance, microbial counts, ileum microscopic anatomy and the expression of inflammatory mediators in weaned piglets following an Escherichia coli infection. Animal Feed Science and Technology 209, 219–229.
Influence of a blend of essential oils and an enzyme combination on growth performance, microbial counts, ileum microscopic anatomy and the expression of inflammatory mediators in weaned piglets following an Escherichia coli infection.Crossref | GoogleScholarGoogle Scholar |

Jørgensen JN, Laguna JS, Millán C, Casabuena O, Gracia MI (2016) Effects of a Bacillus-based probiotic and dietary energy content on the performance and nutrient digestibility of wean to finish pigs. Animal Feed Science and Technology 221, 54–61.
Effects of a Bacillus-based probiotic and dietary energy content on the performance and nutrient digestibility of wean to finish pigs.Crossref | GoogleScholarGoogle Scholar |

Kohn RA, Dinneen MM, Russek-Cohen E (2005) Using blood urea nitrogen to predict nitrogen excretion and efficiency of nitrogen utilization in cattle, sheep, goats, horses, pigs, and rats. Journal of Animal Science 83, 879–889.
Using blood urea nitrogen to predict nitrogen excretion and efficiency of nitrogen utilization in cattle, sheep, goats, horses, pigs, and rats.Crossref | GoogleScholarGoogle Scholar | 15753344PubMed |

Kyriakis SC, Tsiloyiannis VK, Vlemmas J, Sarris K, Tsinas AC, Alexopoulos C, Jansegers L (1999) The effect of probiotic LSP 122 on the control of post-weaning diarrhoea syndrome of piglets. Research in Veterinary Science 67, 223–228.
The effect of probiotic LSP 122 on the control of post-weaning diarrhoea syndrome of piglets.Crossref | GoogleScholarGoogle Scholar | 10607501PubMed |

Lallès JP, Boudry G, Favier C, Le Floc’h N, Luron I, Montagne L, Osawald IP, Pie S, Piel C, Séve B (2004) Gut function and dysfunction in young pigs: physiology. Animal Research 53, 301–316.
Gut function and dysfunction in young pigs: physiology.Crossref | GoogleScholarGoogle Scholar |

Lallès JP, Bosi P, Smidt H, Stokes CR (2007) Weaning – a challenge to gut physiologists. Livestock Science 108, 82–93.
Weaning – a challenge to gut physiologists.Crossref | GoogleScholarGoogle Scholar |

Lan RX, Li TS, Kim IH (2016) Effects of essential oils supplementation in different nutrient densities on growth performance, nutrient digestibility, blood characteristics and fecal microbial shedding in weaning pigs. Animal Feed Science and Technology 214, 77–85.
Effects of essential oils supplementation in different nutrient densities on growth performance, nutrient digestibility, blood characteristics and fecal microbial shedding in weaning pigs.Crossref | GoogleScholarGoogle Scholar |

Lee SH, Ingale SL, Kim JS, Kim KH, Lokhande A, Kim EK, Kwon IK, Kim YH, Chae BJ (2014) Effects of dietary supplementation with Bacillus subtilis LS 1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig. Animal Feed Science and Technology 188, 102–110.
Effects of dietary supplementation with Bacillus subtilis LS 1–2 fermentation biomass on growth performance, nutrient digestibility, cecal microbiota and intestinal morphology of weanling pig.Crossref | GoogleScholarGoogle Scholar |

Li P, Piao X, Ru Y, Han X, Xue L, Zhang H (2012a) Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health. Asian-Australasian Journal of Animal Sciences 25, 1617–1626.
Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response and intestinal health.Crossref | GoogleScholarGoogle Scholar | 25049525PubMed |

Li SY, Ru YJ, Liu M, Xu B, Péron A, Shi XG (2012b) The effect of essential oils on performance, immunity and gut microbial population in weaner pigs. Livestock Science 145, 119–123.
The effect of essential oils on performance, immunity and gut microbial population in weaner pigs.Crossref | GoogleScholarGoogle Scholar |

Michiels J, Missotten J, Van Hoorick A, Ovyn A, Fremaut D, De Smet S, Dierick N (2010) Effects of dose and formulation of carvacrol and thymol on bacteria and some functional traits of the gut in piglets after weaning. Archives of Animal Nutrition 64, 136–154.
Effects of dose and formulation of carvacrol and thymol on bacteria and some functional traits of the gut in piglets after weaning.Crossref | GoogleScholarGoogle Scholar | 20481352PubMed |

Nguyen NT, Nguyen HM, Nguyen CV, Nguyen TV, Nguyen MT, Thai HQ, Ho MH, Thwaites G, Ngo HT, Baker S (2016) Use of colistin and other critical antimicrobials on pig and chicken farms in Southern Vietnam and its association with resistance in commensal Escherichia coli bacteria Applied and Environmental Microbiology 82, 3727–3735.
Use of colistin and other critical antimicrobials on pig and chicken farms in Southern Vietnam and its association with resistance in commensal Escherichia coli bacteriaCrossref | GoogleScholarGoogle Scholar | 27084016PubMed |

Oh SY, Yun W, Lee JH, Lee CH, Kwak WK, Cho JH (2017) Effects of essential oil (blended and single essential oils) on anti-biofilm formation of Salmonella and Escherichia coli. Journal of Animal Science and Technology 59, 4
Effects of essential oil (blended and single essential oils) on anti-biofilm formation of Salmonella and Escherichia coli.Crossref | GoogleScholarGoogle Scholar | 28239484PubMed |

Poulsen A-SR, Jonge NDd,, Nielsen JL, Højberg O, Lauridsen C, Cutting SM, Canibe N (2018) Impact of Bacillus spp. spores and gentamicin on the gastrointestinal microbiota of suckling and newly weaned piglets. PLoS One 13, e0207382
Impact of Bacillus spp. spores and gentamicin on the gastrointestinal microbiota of suckling and newly weaned piglets.Crossref | GoogleScholarGoogle Scholar |

Rhouma M, Fairbrother JM, Beaudry F, Letellier A (2017) Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies. Acta Veterinaria Scandinavica 59, 31
Post weaning diarrhea in pigs: risk factors and non-colistin-based control strategies.Crossref | GoogleScholarGoogle Scholar | 28526080PubMed |

Ri CS, Jiang XR, Kim MH, Wang J, Zhang HJ, Wu SG, Bontempo V, Qi GH (2017) Effects of dietary oregano powder supplementation on the growth performance, antioxidant status and meat quality of broiler chicks. Italian Journal of Animal Science 16, 246–252.
Effects of dietary oregano powder supplementation on the growth performance, antioxidant status and meat quality of broiler chicks.Crossref | GoogleScholarGoogle Scholar |

Ronquillo MG, Hernandez JCA (2017) Antibiotic and synthetic growth promoters in animal diets: Review of impact and analytical methods. Food Control 72, 255–267.
Antibiotic and synthetic growth promoters in animal diets: Review of impact and analytical methods.Crossref | GoogleScholarGoogle Scholar |

Trevisi P, Merialdi G, Mazzoni M, Casini L, Tittarelli C, De Filippi S, Minieri L, Lalatta-Costerbosa G, Bosi P, Trevisi P (2007) Effect of dietary addition of thymol on growth, salivary and gastric function, immune response, and excretion of Salmonella enterica serovar Typhimurium, in weaning pigs challenged with this microbe strain. Italian Journal of Animal Science 6, 374–376.
Effect of dietary addition of thymol on growth, salivary and gastric function, immune response, and excretion of Salmonella enterica serovar Typhimurium, in weaning pigs challenged with this microbe strain.Crossref | GoogleScholarGoogle Scholar |

Upadhaya SD, Kim SC, Valientes RA, Kim IH (2015) The effect of Bacillus-based feed additive on growth performance, nutrient digestibility, fecal gas emission, and pen cleanup characteristics of growing-finishing pigs. Asian-Australasian Journal of Animal Sciences 28, 999–1005.
The effect of Bacillus-based feed additive on growth performance, nutrient digestibility, fecal gas emission, and pen cleanup characteristics of growing-finishing pigs.Crossref | GoogleScholarGoogle Scholar | 26104405PubMed |

Varel VH (2002) Carvacrol and thymol reduce swine waste odor and pathogens: stability of oils. Current Microbiology 44, 38–43.
Carvacrol and thymol reduce swine waste odor and pathogens: stability of oils.Crossref | GoogleScholarGoogle Scholar | 11727039PubMed |

Wei H-K, Xue H-X, Zhou ZX, Peng J (2017) A carvacrol–thymol blend decreased intestinal oxidative stress and influenced selected microbes without changing the messenger RNA levels of tight junction proteins in jejunal mucosa of weaning piglets. Animal 11, 193–201.
A carvacrol–thymol blend decreased intestinal oxidative stress and influenced selected microbes without changing the messenger RNA levels of tight junction proteins in jejunal mucosa of weaning piglets.Crossref | GoogleScholarGoogle Scholar | 27416730PubMed |

Xu YT, Liu L, Long SF, Pan L, Piao XS (2018) Effect of organic acids and essential oils on performance, intestinal health and digestive enzyme activities of weaned pigs. Animal Feed Science and Technology 235, 110–119.
Effect of organic acids and essential oils on performance, intestinal health and digestive enzyme activities of weaned pigs.Crossref | GoogleScholarGoogle Scholar |

Yan L, Wang JP, Kim HJ, Meng QW, Ao X, Hong SM, Kim IH (2010) Influence of essential oil supplementation and diets with different nutrient densities on growth performance, nutrient digestibility, blood characteristics, meat quality and fecal noxious gas content in grower–finisher pigs. Livestock Science 128, 115–122.
Influence of essential oil supplementation and diets with different nutrient densities on growth performance, nutrient digestibility, blood characteristics, meat quality and fecal noxious gas content in grower–finisher pigs.Crossref | GoogleScholarGoogle Scholar |

Zhang W, Zhu YH, Zhou D, Wu Q, Song D, Dicksved J, Wang JF (2017) Oral administration of a select mixture of Bacillus probiotics affects the gut microbiota and goblet cell function following Escherichia coli challenge in newly weaned pigs of genotype MUC4 that are supposed to be enterotoxigenic E. coli F4ab/ac receptor negative. Environmental Microbiology 83, 2747–2763.

Zhao PY, Kim IH (2015) Effect of direct-fed microbial on growth performance, nutrient digestibility, fecal noxious gas emission, fecal microbial flora and diarrhea score in weanling pigs. Animal Feed Science and Technology 200, 86–92.
Effect of direct-fed microbial on growth performance, nutrient digestibility, fecal noxious gas emission, fecal microbial flora and diarrhea score in weanling pigs.Crossref | GoogleScholarGoogle Scholar |

Zhu X, Liu W, Yuan S, Chen H (2014) The effect of different dietary levels of thyme essential oil on serum biochemical indices in Mahua broiler chickens. Italian Journal of Animal Science 13, 3238
The effect of different dietary levels of thyme essential oil on serum biochemical indices in Mahua broiler chickens.Crossref | GoogleScholarGoogle Scholar |

Zou Y, Xiang Q, Wang J, Peng J, Wei H (2016) Oregano essential oil improves intestinal morphology and expression of tight junction proteins associated with modulation of selected intestinal bacteria and immune status in a pig model. BioMed Research International 2016, 1–11.
Oregano essential oil improves intestinal morphology and expression of tight junction proteins associated with modulation of selected intestinal bacteria and immune status in a pig model.Crossref | GoogleScholarGoogle Scholar |