Antimicrobials added to the feed of weaned piglets at two ages improves the molecular expression of intestinal barrier proteins
Victor H. Herrera Franco
A * , Sandra C. Pardo Carrasco A and Jaime E. Parra Suescún A
+ Author Affiliations
- Author Affiliations
A Facultad de Ciencias Agrarias, Departamento de Producción Animal, Universidad Nacional de Colombia, sede Medellín, Medellín, Colombia.
Animal Production Science 62(6) 511-520 https://doi.org/10.1071/AN21027
Submitted: 2 February 2021 Accepted: 27 December 2021 Published: 22 February 2022
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Context: Weaning is the most critical period during a pig’s life, because it is a challenge with the change of environment, and the digestive system is not adapted to a solid diet at the time of weaning, favouring the appearance of intestinal disorders, infections and diarrhoea.
Aims: To quantify the gene abundance of intestinal barrier tight junction proteins in pigs fed diets added with antimicrobials and weaned at two ages.
Methods: A total of 150 pigs weaned at two ages (21 and 28 days) were distributed into groups: Control Diet 1 (D1-Ctrl) without antimicrobial; Diet 2 (D2-Ant): Ctrl with an antibiotic (bacitracin zinc); Diet 3 (D3-Prob): Ctrl with Bacillus subtilis PB6 (PTA-6737); Diet 4 (D4-OEO): Ctrl with oregano essential oil (OEO; Lippia origanoides); Diet 5 (D5-OA): Ctrl with a mixture of organic acids. On post-weaning Days 1, 15 and 30, pigs were euthanised, and a portion of the jejunum was removed to assess the gene abundance of the intestinal tight junction proteins (occludin-OCLN, zonula occludens-ZO-1 and claudins-CLAU) that were measured by qPCR.
Key results: The pigs fed the diet with the addition of D3-Prob and D4-OEO showed a higher abundance (P < 0.05) of intestinal barrier tight junction protein genes (CLAU-1, CLAU-4, OCLN, ZO-1) compared with the other diets. This abundance was observed in both piglets weaned early, at 21 days, and later at 28 days of age, where, in addition, a statistically significant difference between weaning ages (P < 0.05) was evidenced in favour of later weaning.
Conclusions: The addition of probiotics in the growth phase, together with weaning at 28 days of age, have a favourable impact on the intestinal digestive function of pigs, being able to influence morphometric and productive parameters, and serve as a basis for the analysis of molecular research related to intestinal health.
Implications: This research provides a basis for the use of natural nutritional alternatives, such as probiotic bacteria, as alternatives to growth-promoting antibiotics in the feed of growing pigs; in addition to encouraging a better adaptation of the piglet to the post-weaning phase, through late weaning.
Keywords: growth promoting antibiotic, intestinal barrier, oregano essential oil, probiotic, protein expression, swine, tight junction proteins, weaning.
References
Begum M, Hossain MM, Kim IH (2016) Effects of fenugreek seed extract supplementation on growth performance, nutrient digestibility, diarrhoea scores, blood profiles, faecal microflora and faecal noxious gas emission in weanling piglets. Journal of Animal Physiology and Animal Nutrition 100, 1121–1129.| Effects of fenugreek seed extract supplementation on growth performance, nutrient digestibility, diarrhoea scores, blood profiles, faecal microflora and faecal noxious gas emission in weanling piglets.Crossref | GoogleScholarGoogle Scholar | 26947773PubMed |
Campbell JM, Crenshaw JD, Polo J (2013) The biological stress of early weaned piglets. Journal of Animal Science and Biotechnology 4, 19
| The biological stress of early weaned piglets.Crossref | GoogleScholarGoogle Scholar | 23631414PubMed |
Chen H, Mao X, He J, Yu B, Huang Z, Yu J, Zheng P, Chen D (2013) Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets. British Journal of Nutrition 110, 1837–1848.
| Dietary fibre affects intestinal mucosal barrier function and regulates intestinal bacteria in weaning piglets.Crossref | GoogleScholarGoogle Scholar |
Cho JH, Kim IH (2015) Effects of microencapsulated organic acids and essential oils on growth performance and intestinal flora in weanling pigs. Revista Colombiana de Ciencias Pecuarias 28, 229–237.
| Effects of microencapsulated organic acids and essential oils on growth performance and intestinal flora in weanling pigs.Crossref | GoogleScholarGoogle Scholar |
Ciro Galeano JA, López Herrera A, Parra Suescún J (2015) La adición de cepas probióticas modula la secreción de mucinas intestinales en íleon de cerdos en crecimiento (Addition of probiotic strains modulates intestinal mucin secretion of the ileum of growing pigs). Revista CES Medicina Veterinaria y Zootecnia 10, 150–159.
| La adición de cepas probióticas modula la secreción de mucinas intestinales en íleon de cerdos en crecimiento (Addition of probiotic strains modulates intestinal mucin secretion of the ileum of growing pigs).Crossref | GoogleScholarGoogle Scholar |
Ciro Galeano JA, López Herrera A, Parra Suescún J (2016) The probiotic Enterococcus faecium modifies the intestinal morphometric parameters in weaning piglets. Revista Facultad Nacional de Agronomía 69, 7803–7811.
| The probiotic Enterococcus faecium modifies the intestinal morphometric parameters in weaning piglets.Crossref | GoogleScholarGoogle Scholar |
Ecco R, Brown C, Susta L, Cagle C, Cornax I, Pantin-Jackwood M, Miller PJ, Afonso CL (2011) In vivo transcriptional cytokine responses and association with clinical and pathological outcomes in chickens infected with different Newcastle disease virus isolates using formalin-fixed paraffin-embedded samples. Veterinary Immunology and Immunopathology 141, 221–229.
| In vivo transcriptional cytokine responses and association with clinical and pathological outcomes in chickens infected with different Newcastle disease virus isolates using formalin-fixed paraffin-embedded samples.Crossref | GoogleScholarGoogle Scholar | 21458080PubMed |
FAO/WHO (Food and Agriculture Organization/World Health Organization) (2001) Health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. Report of a joint FAO/WHO expert consultation on evaluation of health and nutritional properties of probiotics in food including powder milk with live lactic acid bacteria. FAO/WHO: Córdoba, Argentina. p. 1–33.
Felipe Patiño F, Víctor Herrera F, Daniela López D, Jaime Parra S (2019) Blood metabolites and zootechnical parameters in piglets weaned at two ages and with the addition of antimicrobials in the feed. Revista de Investigaciones Veterinarias del Perú 30, 612–623.
| Blood metabolites and zootechnical parameters in piglets weaned at two ages and with the addition of antimicrobials in the feed.Crossref | GoogleScholarGoogle Scholar |
Gutiérrez LA, Montoya OI, Vélez JMZ (2013) Probióticos: una alternativa de producción limpia y de reemplazo a los antibióticos promotores de crecimiento en la alimentación animal (Probiotics: a green production and replacement alternative to growth promoting antibiotics in animal feed). Producción + Limpia 8, 135–146.
Hu CH, Xiao K, Luan ZS, Song J (2013) Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs. Journal of Animal Science 91, 1094–1101.
| Early weaning increases intestinal permeability, alters expression of cytokine and tight junction proteins, and activates mitogen-activated protein kinases in pigs.Crossref | GoogleScholarGoogle Scholar | 23230104PubMed |
Hu Q, Li S, Zhang Y, Zhuo Z, Feng J (2017) Phytosterols on growth performance, antioxidant enzymes and intestinal morphology in weaned piglets. Journal of the Science of Food and Agriculture 97, 4629–4634.
| Phytosterols on growth performance, antioxidant enzymes and intestinal morphology in weaned piglets.Crossref | GoogleScholarGoogle Scholar | 28349555PubMed |
Hu S, Cao X, Wu Y, Mei X, Xu H, Wang Y, Zhang X, Gong L, Li W (2018) Effects of probiotic bacillus as an alternative of antibiotics on digestive enzymes activity and intestinal integrity of piglets. Frontiers in Microbiology 9, 2427
| Effects of probiotic bacillus as an alternative of antibiotics on digestive enzymes activity and intestinal integrity of piglets.Crossref | GoogleScholarGoogle Scholar | 30405544PubMed |
ICLAS (2012) International guiding principles for biomedical research involving animals. Council for International Organization of Medical Sciences and the International Council for Laboratory Animal Science.
Kim YS, Ho SB (2010) Intestinal goblet cells and mucins in health and disease: recent insights and progress. Current Gastroenterology Reports 12, 319–330.
| Intestinal goblet cells and mucins in health and disease: recent insights and progress.Crossref | GoogleScholarGoogle Scholar | 20703838PubMed |
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 |
López-Vergé S, Gasa J, Coma J, Bonet J, Solà-Oriol D (2019) Effect of lactation length caused by the management production system on piglet performance until slaughter. Livestock Science 224, 26–30.
| Effect of lactation length caused by the management production system on piglet performance until slaughter.Crossref | GoogleScholarGoogle Scholar |
Ma Y, Semba S, Khan MRI, Bochimoto H, Watanabe T, Fujiya M, Kohgo Y, Liu Y, Taniguchi T (2013) Focal adhesion kinase regulates intestinal epithelial barrier function via redistribution of tight junction. Biochimica et Biophysica Acta (BBA) - Molecular Basis of Disease 1832, 151–159.
| Focal adhesion kinase regulates intestinal epithelial barrier function via redistribution of tight junction.Crossref | GoogleScholarGoogle Scholar |
Madrid-Garcés TA, López-Herrera A, Parra-Suescún JE (2018) La ingesta de aceite esencial de orégano (Lippia origanoides) mejora la morfología intestinal en Broilers. Archivos de Zootecnia 67, 470–476.
| La ingesta de aceite esencial de orégano (Lippia origanoides) mejora la morfología intestinal en Broilers.Crossref | GoogleScholarGoogle Scholar |
Mariani V, Palermo S, Fiorentini S, Lanubile A, Giuffra E (2009) Gene expression study of two widely used pig intestinal epithelial cell lines: IPEC-J2 and IPI-2I. Veterinary Immunology and Immunopathology 131, 278––284.
| Gene expression study of two widely used pig intestinal epithelial cell lines: IPEC-J2 and IPI-2I.Crossref | GoogleScholarGoogle Scholar | 19446887PubMed |
Michiels J, Possemiers S, Degroote J, Ovyn A, De Smet S, Nakamura N (2016) Feeding Bacillus subtilis C-3102 to sows and suckling piglets and to weaned piglets improves parameters of gut health and feed:gain ratio in weaners. Journal of Animal Science 94, 135–137.
| Feeding Bacillus subtilis C-3102 to sows and suckling piglets and to weaned piglets improves parameters of gut health and feed:gain ratio in weaners.Crossref | GoogleScholarGoogle Scholar |
Moeser AJ, Ryan KA, Nighot PK, Blikslager AT (2007) Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs. American Journal of Physiology-Gastrointestinal and Liver Physiology 293, G413–G421.
| Gastrointestinal dysfunction induced by early weaning is attenuated by delayed weaning and mast cell blockade in pigs.Crossref | GoogleScholarGoogle Scholar | 17525151PubMed |
Mota RD, Roldán SP, Pérez PE, Martínez RR, Hernández TE, Trujillo OME (2014) Stress factors in weaned piglet. Veterinaria México 1, 37–51.
National Research Council (U.S.) (2012) ‘Nutrient requirements of swine.’, 11th edn. (The National Academies Press: Washington, DC)
Ospina D, Ciro J, Román Y, Peláez C, López A, Parra J (2011) Cambios en la actividad enzimática en duodeno y yeyuno de cerdos durante varios periodos posdestete (Changes in enzyme activity in duodenum and jejunum of pigs during various post-weaning periods). Revista de la Facultad de Medicina Veterinaria y de Zootecnia 58, 156–165.
Papatsiros VG, Tassis PD, Tzika ED, Papaioannou DS, Petridou E, Alexopoulos C, Kyriakis SC (2011) Effect of benzoic acid and combination of benzoic acid with a probiotic containing Bacillus cereus var. Toyoi in weaned pig nutrition. Polish Journal of Veterinary Sciences 14, 117–125.
| Effect of benzoic acid and combination of benzoic acid with a probiotic containing Bacillus cereus var. Toyoi in weaned pig nutrition.Crossref | GoogleScholarGoogle Scholar | 21528721PubMed |
Patiño F (2018) Utilización de compuestos antimicrobianos en cerdos destetados a dos edades y su efecto sobre parámetros zootécnicos, metabólicos e intestinales (Use of antimicrobial compounds in weaned pigs at two ages and their effect on zootechnical, metabolic and intestinal parameters). Tesis Maestría, Universidad Nacional de Colombia, Facultad de Ciencias Agrarias, Medellín, Colombia.
Placha I, Takacova J, Ryzner M, Cobanova K, Laukova A, Strompfova V, Venglovska K, Faix S (2014) Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers. British Poultry Science 55, 105–114.
| Effect of thyme essential oil and selenium on intestine integrity and antioxidant status of broilers.Crossref | GoogleScholarGoogle Scholar | 24397472PubMed |
Rahn E, Thier K, Petermann P, Rübsam M, Staeheli P, Iden S, Niessen CM, Knebel-Mörsdorf D (2017) Epithelial barriers in murine skin during herpes simplex virus 1 infection: the role of tight junction formation. Journal of Investigative Dermatology 137, 884–893.
| Epithelial barriers in murine skin during herpes simplex virus 1 infection: the role of tight junction formation.Crossref | GoogleScholarGoogle Scholar |
Robinson K, Deng Z, Hou Y, Zhang G (2015) Regulation of the intestinal barrier function by host defense peptides. Frontiers in Veterinary Science 2, 57
| Regulation of the intestinal barrier function by host defense peptides.Crossref | GoogleScholarGoogle Scholar | 26664984PubMed |
SAS/STAT (2017) SAS® SAS/STAT User’s Guide, Version 14.3th Ed. (SAS Institute Inc: Cary, NC) Available at https://www.sas.com/content/dam/SAS/en_us/doc/factsheet/stat-101372.pdf
Segalés J, Domingo M (2003) ‘La necropsia en el ganado porcino diagnóstico anatomopatológico y toma de muestras (Necropsy in swine cattle pathological diagnosis and sampling).’ (Boehringer Ingelheim: Barcelona, Spain)
Spreeuwenberg MAM, Verdonk JMAJ, Gaskins HR, Verstegen MWA (2001) Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning. The Journal of Nutrition 131, 1520–1527.
| Small intestine epithelial barrier function is compromised in pigs with low feed intake at weaning.Crossref | GoogleScholarGoogle Scholar |
Su S, Miska KB, Fetterer RH, Jenkins MC, Wong EA (2014) Expression of digestive enzymes and nutrient transporters in Eimeria acervulina-challenged layers and broilers. Poultry Science 93, 1217–1226.
| Expression of digestive enzymes and nutrient transporters in Eimeria acervulina-challenged layers and broilers.Crossref | GoogleScholarGoogle Scholar | 24795315PubMed |
Su S, Miska KB, Fetterer RH, Jenkins MC, Wong EA (2015) Expression of digestive enzymes and nutrient transporters in Eimeria-challenged broilers. Experimental Parasitology 150, 13–21.
| Expression of digestive enzymes and nutrient transporters in Eimeria-challenged broilers.Crossref | GoogleScholarGoogle Scholar | 25617757PubMed |
Suzuki T (2013) Regulation of intestinal epithelial permeability by tight junctions. Cellular and Molecular Life Sciences 70, 631–659.
| Regulation of intestinal epithelial permeability by tight junctions.Crossref | GoogleScholarGoogle Scholar | 22782113PubMed |
Tang W, Qian Y, Yu B, Zhang T, Gao J, He J, Huang Z, Zheng P, Mao X, Luo J, Yu J, Chen D (2019) Effects of Bacillus subtilis DSM32315 supplementation and dietary crude protein level on performance, gut barrier function and microbiota profile in weaned piglets. Journal of Animal Science 97, 2125–2138.
| Effects of Bacillus subtilis DSM32315 supplementation and dietary crude protein level on performance, gut barrier function and microbiota profile in weaned piglets.Crossref | GoogleScholarGoogle Scholar | 30883644PubMed |
Thacker PA (2013) Alternatives to antibiotics as growth promoters for use in swine production: a review. Journal of Animal Science and Biotechnology 4, 35
| Alternatives to antibiotics as growth promoters for use in swine production: a review.Crossref | GoogleScholarGoogle Scholar | 24034214PubMed |
Upadhaya SD, Lee KY, Kim IH (2014) Protected organic Acid blends as an alternative to antibiotics in finishing pigs. Asian-Australasian Journal of Animal Science 27, 1600–1607.
| Protected organic Acid blends as an alternative to antibiotics in finishing pigs.Crossref | GoogleScholarGoogle Scholar |
van der Meulen J, Koopmans SJ, Dekker RA, Hoogendoorn A (2010) Increasing weaning age of piglets from 4 to 7 weeks reduces stress, increases post-weaning feed intake but does not improve intestinal functionality. Animal 4, 1653–1661.
| Increasing weaning age of piglets from 4 to 7 weeks reduces stress, increases post-weaning feed intake but does not improve intestinal functionality.Crossref | GoogleScholarGoogle Scholar | 22445118PubMed |
Vega R, Estrella C, Valera A, Calud A, Villar E (2012) Performance of selected Philippine commercial piggery farms weaning at different ages. Philippine Journal of Veterinary and Animal Sciences 38, 127–133.
Wang J, Ji H (2019) Tight junction proteins in the weaned piglet intestine: roles and regulation. Current Protein & Peptide Science 20, 652–660.
| Tight junction proteins in the weaned piglet intestine: roles and regulation.Crossref | GoogleScholarGoogle Scholar |
Wang J, Wu Z, Li D, Li N, Dindot SV, Satterfield MC, Bazer FW, Wu G (2012) Nutrition, epigenetics, and metabolic syndrome. Antioxidants & Redox Signaling 17, 282–301.
| Nutrition, epigenetics, and metabolic syndrome.Crossref | GoogleScholarGoogle Scholar |
Wijtten PJA, Meulen J, Verstegen MWA (2011) Intestinal barrier function and absorption in pigs after weaning: a review. British Journal of Nutrition 105, 967–981.
| Intestinal barrier function and absorption in pigs after weaning: a review.Crossref | GoogleScholarGoogle Scholar |
Xiao K, Song Z-H, Jiao L-F, Ke Y-L, Hu C-H (2014) Developmental changes of TGF-β1 and smads signaling pathway in intestinal adaption of weaned pigs. PLoS ONE 9, e104589
| Developmental changes of TGF-β1 and smads signaling pathway in intestinal adaption of weaned pigs.Crossref | GoogleScholarGoogle Scholar | 25170924PubMed |
Xun W, Shi L, Zhou H, Hou G, Cao T (2018) Effect of weaning age on intestinal mucosal morphology, permeability, gene expression of tight junction proteins, cytokines and secretory IgA in Wuzhishan mini piglets. Italian Journal of Animal Science 17, 976–983.
| Effect of weaning age on intestinal mucosal morphology, permeability, gene expression of tight junction proteins, cytokines and secretory IgA in Wuzhishan mini piglets.Crossref | GoogleScholarGoogle Scholar |
Yang H, Xiong X, Wang X, Tan B, Li T, Yin Y (2016) Effects of weaning on intestinal upper villus epithelial cells of piglets. PLoS ONE 11, 1–20.
| Effects of weaning on intestinal upper villus epithelial cells of piglets.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, 5436738
| 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 | 27314026PubMed |
