Planta Med 2022; 88(03/04): 324-335
DOI: 10.1055/a-1698-8469
Biological and Pharmacological Activity
Original Papers

Effect of Dietary Oregano (Lippia origanoides) and Clover (Eugenia caryophillata) Essential Oilsʼ Formulations on Intestinal Health and Performance of Pigs

Susana Nelly Dieguez
1   Área Toxicología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
4   Comisión de Investigaciones Científicas de la Provincia de Buenos Aires (CIC-PBA), Tandil, Argentina
,
1   Área Toxicología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
,
Guadalupe Martínez
1   Área Toxicología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
,
Fabián Andrés Amanto
3   Área Producción Porcina, Departamento de Producción Animal, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
,
Carolina Paula Bianchi
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
5   Área Endocrinología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
,
Denisa Soledad Pérez Gaudio
1   Área Toxicología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
,
Alejandro Luis Soraci
1   Área Toxicología, Departamento de Fisiopatología, Facultad de Ciencias Veterinarias, Universidad Nacional del Centro de la Provincia de Buenos Aires, Tandil, Argentina
2   Facultad de Ciencias Veterinarias, Centro de Investigación Veterinaria de Tandil (CIVETAN), UNCPBA-CICPBA-CONICET, Tandil, Argentina
› Institutsangaben
Gefördert durch: Consejo Nacional de Investigaciones Científicas y Técnicas

Abstract

The incorporation of natural essential oils to the pigsʼ diet in intensive production systems is a potential tool to improve gut health and prevent infections without using antibiotics. Nevertheless, different products, even containing the same compounds, coming from the same botanical species, may exert dissimilar biological effects due differences in the technological processes by which they are produced and preserved. For this reason, suitability of a given product based on natural extracts, intended for swine production must be thoroughly evaluated. In the present study, we assessed the effects of three additives containing oregano (Lippia origanoides) essential oil, alone or in combination with clover (Eugenia caryophillata) essential oil, with or without being microencapsulated, on gastrointestinal health and on some performance parameters in a commercial pig production farm. Recently weaned piglets were randomly divided in four groups, and basal diet or essential oil-supplemented diet (OCE; MOCE; MOE) was randomly assigned to each of the groups from weaning to finishing. Blood samples were collected at pre-established days after weaning. Intestinal sampling took place at 42 and 72 days of age. Pigs consuming the supplemented diets showed higher intestinal metabolic activity during the post-weaning period, decreasing the impact of weaning stress on enterocytesʼ metabolism. Intestinal barrier function was not affected in pigs consuming microencapsulated products. All treated groups showed improved intestinal architecture, increased digestive enzymes activity and caecal VFA concentrations. The incorporation of the dietary essential oils products brought beneficial effects on gastrointestinal health that were reflected in improved performance parameters.



Publikationsverlauf

Eingereicht: 06. April 2021

Angenommen nach Revision: 11. November 2021

Artikel online veröffentlicht:
16. Dezember 2021

© 2021. Thieme. All rights reserved.

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  • References

  • 1 Pradella G, Anadon A, Klose V, Plalil R, Mohnl M, Schatzmayr G, Spring P, Montesissa C, Calini F. Workshop III: 2006 EU Ban on antibiotics as feed additives: Consequences and perspectives. J Vet Pharmacol Therap 2006; 29: 41-46
  • 2 Yang C, Chowdhury MA, Huo Y, Gon J. Phytogenic compounds as alternatives to in-feed antibiotics: Potentials and challenges in application. Pathogens 2015; 4: 137-156
  • 3 Omonijo FA, Ni L, Gong J, Wang Q, Lahaye L, Yang C. Essential oils as alternatives to antibiotics in swine production. Anim Nutr 2018; 4: 126-136
  • 4 European Commission. Regulation (EU) 2019/4 of the European Parliament and of the Council of 11 December 2018 on the manufacture, placing on the market and use of medicated feed, amending regulation (EC) NO 183/2005 of the European Parliament and of the Council and repealing Council Directive 90/167/EEC (text with EEA relevance). OJEU 2019; 4: 1-23
  • 5 Lekagul A, Tangcharoensathien V, Yeung S. Patterns of antibiotic use in global pig production: A systematic review. Vet Anim Sci 2019; 7: 100058
  • 6 Campbell JM, Crenshaw JD, Polo J. The biological stress of early weaned piglets. J Anim Sci Biotechnol 2013; 4: 2-5 DOI: 10.1186/2049-1891-4-19.
  • 7 Heo JM, Opapeju FO, Pluske JR, Kim JC, Hampson DJ, Nyachoti CM. Gastrointestinal health and function in weaned pigs: A review of feeding strategies to control post-weaning diarrhoea without using in-feed antimicrobial compounds. J Anim Physiol An N 2013; 97: 207-237
  • 8 Zhai H, Liu H, Wang S, Wu J, Kluenter AM. Potential of essential oils for poultry and pigs. Anim Nutr 2018; 4: 179-186
  • 9 Franz C, Baser KHC, Windisch W. Essential oils and aromatic plants in animal feeding–a European perspective. A review. Flavour Fragr J 2010; 25: 327-340
  • 10 Kroismayr A, Sehm J, Pfaffl MW, Schedle K, Plitzner C, Windisch W. Effects of avilamycin and essential oils on mRNA expression of apoptotic and inflammatory markers and gut morphology of piglets. Czech J Anim Sci 2008; 53: 377-387
  • 11 Gandhi GR, Vasconcelos ABS, Haran GH, Calisto VKS, Jothi G, Quintans JDSS, Gurgel RQ. Essential oils and its bioactive compounds modulating cytokines: A systematic review on anti-asthmatic and immunomodulatory properties. Phytomedicine 2020; 73: 152854
  • 12 Li P, Piao X, Ru Y, Han X, Xue L, Zhang H. Effects of adding essential oil to the diet of weaned pigs on performance, nutrient utilization, immune response, and intestinal health. Asian Australas J Anim Sci 2012; 25: 1617
  • 13 Németh-Zámboriné E. Natural Variability of essential Oil Components. In: Can Baser KH, Buchbauer G. eds. Essential Oils: Science, Technology, and Applications. Boca Raton: CRC Press; 2016: 87-125
  • 14 Stevanović ZD, Bošnjak-Neumüller J, Pajić-Lijaković I, Raj J, Vasiljević M. Essential oils as feed additives–future perspectives. Molecules 2018; 23: 1717
  • 15 Chitprasert P, Sutaphanit P. Holy basil (Ocimum sanctum Linn.) essential oil delivery to swine gastrointestinal tract using gelatin microcapsules coated with aluminum carboxymethyl cellulose and beeswax. J Agric Food Chem 2014; 62: 12641-12648
  • 16 Wang Q, Gong J, Huang X, Yu H, Xue F. In vitro evaluation of the activity of microencapsulated carvacrol against Escherichia coli with K88 pili. J Appl Microbiol 2009; 107: 1781-1788
  • 17 Marion J, Biernat M, Savary G, Thomas F, Zabielski R. Le Huërou-Luron I. Le Dividich J. Effet dʼun sevrage à lʼâge de 7 jours et du niveau alimentaire après le sevrage sur les modifications structurales de lʼintestin grêle chez le porcelet. J Rech Porc Fr 2002; 34: 89-95
  • 18 Al Masri S, Hünigen H, Al Aiyan A, Rieger J, Zentek J, Richardson K, Plendl J. Influence of age at weaning and feeding regimes on the postnatal morphology of the porcine small intestine. J Swine Health Prod 2015; 23: 186-203
  • 19 Tao X, Xu Z, Men X. Transient effects of weaning on the health of newly weaning piglets. Czech J Anim Sci 2016; 61: 82-90
  • 20 Li LA, Yang JJ, Li Y, Lv L, Xie JJ, Du GM, Jiao XL. Effect of weaning age on cortisol release in piglets. Genet Mol Res 2016; 15: 1-10
  • 21 Martínez-Miró S, Tecles F, Ramón M, Escriban D, Hernánde F, Madrid J, Cerón JJ. Causes, consequences and biomarkers of stress in swine: an update. BMC Vet Res 2016; 12: 1-9
  • 22 Berkeveld M, Langendijk P, Verheijden JHM, Taverne MAM, Van Nes A, Van Haard P, Koets AP. Citrulline and intestinal fatty acid-binding protein: Longitudinal markers of postweaning small intestinal function in pigs?. J Anim Sci 2008; 86: 3440-3449
  • 23 Zou Y, Wang J, Peng J, Wei H. Oregano essential oil induces SOD1 and GSH expression through Nrf2 activation and alleviates hydrogen peroxide-induced oxidative damage in IPEC-J2 cells. Oxid Med Cell Longev 2016; 2016: 5987183
  • 24 Wei HK, Xue HX, Zhou ZX, Peng J. 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 2017; 11: 193-201
  • 25 Smith F, Clark JE, Overman BL, Tozel CC, Huang JH, Rivier JE, Moeser AJ. Early weaning stress impairs development of mucosal barrier function in the porcine intestine. Am J Physiol-Gastr L 2010; 298: G352-G363
  • 26 Nabuurs MJA, Hoogendoorn A, Van Zijderveld FG. Effects of weaning and enterotoxigenic Escherichia coli on net absorption in the small intestine of pigs. Res Vet Sci 1994; 56: 379-385
  • 27 Tisserand R, Young R. Essential oil safety-e-book: A guide for health care professionals. Edinburgh: Elsevier Health Sciences; 2013
  • 28 Xu YT, Liu LI, Long SF, Pan L, Piao XS. Effect of organic acids and essential oils on performance, intestinal health and digestive enzyme activities of weaned pigs. Anim Feed Sci Technol 2018; 235: 110-119
  • 29 Su G, Zhou X, Wang Y, Chen D, Chen G, Li Y, He J. Dietary supplementation of plant essential oil improves growth performance, intestinal morphology and health in weaned pigs. J Anim Physiol An N 2019; 104: 579-589
  • 30 Basmacioğlu Malayoğlu H, Baysal Ş, Misirlioğlu Z, Polat M, Yilmaz H, Turan N. Effects of oregano essential oil with or without feed enzymes on growth performance, digestive enzyme, nutrient digestibility, lipid metabolism and immune response of broilers fed on wheat–soybean meal diets. Br Poult Sci 2010; 51: 67-80
  • 31 Forder REA, Howarth GS, Tivey DR, Hughes RJ. Bacterial modulation of small intestinal goblet cells and mucin composition during early posthatch development of poultry. Poult Sci J 2007; 86: 2396-2403
  • 32 Święch E, Tuśnio A, Barszcz M, Taciak M, Siwiak E. Goblet cells and mucus layer in the gut of young pigs: Response to dietary contents of threonine and non-essential amino acids. J Anim Physiol Ann 2019; 103: 894-905
  • 33 Zeinali S, Ghazanfari S, Ebrahimi MA. Mucin2 gene expression in the chicken intestinal goblet cells are affected by dietary essential oils. Bulg J Agric Sci 2017; 23: 134-141
  • 34 Pham VH, Kan L, Huang J, Geng Y, Zhen W, Guo Y, Abbas W, Wang Z. Dietary encapsulated essential oils and organic acids mixture improves gut health in broiler chickens challenged with necrotic enteritis. J Anim Sci Biotechnol 2020; 11: 1-18 DOI: 10.1186/s40104-019-0421-y.
  • 35 Franklin MA, Mathew AG, Vickers JR, Clift RA. Characterization of microbial populations and volatile fatty acid concentrations in the jejunum, ileum, and cecum of pigs weaned at 17 vs. 24 days of age. J Anim Sci 2002; 80: 2904-2910
  • 36 Yang C, Zhang L, Cao G, Feng J, Yue M, Xu Y, Dai B, Han Q, Guo X. Effects of dietary supplementation with essential oils and organic acids on the growth performance, immune system, fecal volatile fatty acids, and microflora community in weaned piglets. J Anim Sci 2019; 97: 133-143
  • 37 Bergman EN. Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiol Rev 1990; 70: 567-590
  • 38 Scheppach W. Effects of short chain fatty acids on gut morphology and function. Gut 1994; 35: S35
  • 39 Williams BA, Verstegen MWA, Tamminga S. Fermentation in the large intestine of single-stomached animals and its relationship to animal health. Nutr Res Rev 2001; 14: 207-227
  • 40 Tian Q, Piao X. Essential oil blend could decrease diarrhea prevalence by improving antioxidative capability for weaned pigs. Animals 2019; 9: 847
  • 41 Cho JH, Song MH, Kim IH. Effect of microencapsulated blends of organic acids and essential oils supplementation on growth performance and nutrient digestibility in finishing pigs. Rev Colomb de Cienc Pecu 2014; 27: 264-272
  • 42 National Research Council; Division on Earth and Life Studies; Board on Agriculture and Natural Resources, Committee on Nutrient Requirements of Swine. Nutrient requirements of swine. 11th rev. ed. Washington, DC: The National Academies Press; 2012
  • 43 Pluschke AM, Williams BA, Zhang D, Anderson ST, Roura E, Gidley MJ. Male grower pigs fed cereal soluble dietary fibres display biphasic glucose response and delayed glycaemic response after an oral glucose tolerance test. PLoS One 2018; 13: e0193137
  • 44 Bischoff SC, Barbara G, Buurman W, Ockhuizen T, Schulzke JD, Serino M, Tilg H, Watson A, Wells JM. Intestinal permeability–a new target for disease prevention and therapy. BMC Gastroenterol 2014; 14: 1-25
  • 45 Wu G, Meininger CJ. Analysis of citrulline, arginine, and methylarginines using high-performance liquid chromatography. Methods Enzymol 2008; 440: 177-189
  • 46 Crenn P, Messing B, Cynober L. Citrulline as a biomarker of intestinal failure due to enterocyte mass reduction. Clin Nutr 2008; 27: 328-339
  • 47 Martínez G, Diéguez SN, Paggi MBF, Riccio MB, Gaudio DSP, Rodríguez E, Soraci AL. Effect of fosfomycin, Cynara scolymus extract, deoxynivalenol and their combinations on intestinal health of weaned piglets. Anim Nutr 2019; 5: 386-395
  • 48 Kisielinski K, Willis S, Prescher A, Klosterhalfen B, Schumpelick V. A simple new method to calculate small intestine absorptive surface in the rat. Clin Exp Med 2002; 2: 131-135
  • 49 Bai X, Liu X, Su Y. Inhibitory effects of intestinal mucus on bacterial adherence to cultured intestinal epithelial cells after surface burns. Chin Med J 2000; 113: 449-450
  • 50 RStudio T. RStudio: Integrated development for R. Boston, MA: RStudio, Inc.; 2015. Accessed April 20, 2020 at: https://www.Rstudio.com