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

Characterising barrier function among regions of the gastrointestinal tract in Holstein steers

G. B. Penner A D , J. R. Aschenbach B , K. Wood A , M. E. Walpole A , R. Kanafany-Guzman A , S. Hendrick C and J. Campbell C
+ Author Affiliations
- Author Affiliations

A Department of Animal and Poultry Science, University of Saskatchewan, Saskatoon, SK S7N 5A8, Canada.

B Institute of Veterinary Physiology, Free University of Berlin, D-14163 Berlin, Germany.

C Department of Large Animal Clinical Sciences, University of Saskatchewan, Saskatoon, SK S7N 5A8, Canada.

D Corresponding author. Email: greg.penner@usask.ca

Animal Production Science 54(9) 1282-1287 https://doi.org/10.1071/AN14285
Submitted: 13 March 2014  Accepted: 18 March 2014   Published: 10 July 2014

Abstract

The objective of this study was to characterise the regional variation in the barrier function of the gastrointestinal tract in Holstein calves using the flux rates of mannitol and inulin as permeability markers and tissue conductance (Gt) as an electrophysiological indicator of barrier function. Six Holstein steer calves (6 months of age) fed a common diet were used. Calves were killed by captive bolt stunning and pithing, and tissues were collected from the rumen, omasum, duodenum, jejunum, ileum, caecum, proximal colon, and distal colon. Tissues were carefully washed using a pre-heated (38.5°C) buffer solution (pH 7.4) saturated with oxygen and then transported to the laboratory. The mucosa was prepared by hand stripping and mounted between two halves of an Ussing chamber (n = 3/region with an exposed surface area of 3.14 cm2 for rumen and omasum and 1 cm2 for all other tissues). All tissues were incubated under short-circuit conditions and exposed to a similar buffer solution except for the energy source; rumen, omasum, caecum, and colon tissues were incubated with buffer containing short-chain fatty acids while tissues from the small intestine were bathed in buffer containing glucose. The Gt and the serosal-to-mucosal flux rates of 14C-inulin and 3H-mannitol were measured as indicators of barrier function. The serosal-to-mucosal flux rate of mannitol was greatest (P < 0.001) in the jejunum [104.8 nmol/(cm2 × h)] and least in the rumen and omasum [20.3 and 18.6 nmol/(cm2 × h), respectively]. In contrast, the serosal-to-mucosal flux rate of inulin was greatest (P < 0.001) in the omasum [158.6 nmol/(cm2 × h)] followed by the rumen [87.3 nmol/(cm2 × h)] with no differences among the other regions [18.7 – 62.0 nmol/(cm2 × h)]. The Gt was greatest (P < 0.001) in the jejunum (34.6 mS/cm2) and least for the rumen (3.67 mS/cm2) and omasum (3.23 mS/cm2). The Gt was correlated with both inulin and mannitol flux rates in duodenum, caecum and proximal colon (P < 0.05); whereas, no such correlations existed in jejunum, ileum and distal colon. The Gt was correlated with the mannitol flux rate but not the inulin flux rate in rumen and omasum. For all regions but the rumen and omasum there was a positive correlation between mannitol and inulin flux rates. These data indicate that the translocation of a large molecule (inulin) across the omasum and rumen is greatest despite having an apparently tight epithelium based on Gt and mannitol flux rate, while the jejunum appears to have greatest potential for paracellular permeability.

Additional keywords: barrier function, gastrointestinal tract, inulin, mannitol, ruminant.


References

Abdoun K, Stumpff F, Rabbani I, Martens H (2010) Modulation of urea transport across sheep rumen epithelium in vitro by SCFA and CO2. American Journal of Physiology. Gastrointestinal and Liver Physiology 298, G190–G202.
Modulation of urea transport across sheep rumen epithelium in vitro by SCFA and CO2.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvVyrs7k%3D&md5=255de38ca449fa46a66be9d84cfee45dCAS | 19926818PubMed |

Aschenbach JR, Ahrens F, Garz B, Gäbel G (2000) Transport, catabolism and release of histamine in the ruminal epithelium of sheep. Pflugers Archiv 440, 171–178.
Transport, catabolism and release of histamine in the ruminal epithelium of sheep.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXjsFKitrc%3D&md5=1284b408488a8c51f0c59aa520df8845CAS | 10864012PubMed |

Aschenbach JR, Penner GB, Stumpff F, Gäbel G (2011) Ruminant nutrition symposium: role of fermentation acid absorption in the regulation of ruminal pH. Journal of Animal Science 89, 1092–1107.
Ruminant nutrition symposium: role of fermentation acid absorption in the regulation of ruminal pH.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXntFKltbo%3D&md5=1c74857dd1fd1405c19cb4b4d864bf5cCAS | 20952531PubMed |

Bergman EN (1990) Energy contributions of volatile fatty acids from the gastrointestinal tract in various species. Physiological Reviews 70, 567–590.

Bjarnason J, Peters TJ (1984) In vitro determination of small intestinal permeability: demonstration of a persistent defect in patients with ceoliac disease. Gut 25, 145–150.
In vitro determination of small intestinal permeability: demonstration of a persistent defect in patients with ceoliac disease.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaL2c7gvFKjtw%3D%3D&md5=087a0c25c3c86b9cc8ff52f9b24bd074CAS |

Gäbel G, Vogler S, Martens H (1991) Short-chain fatty acids and CO2 as regulators of Na+ and Cl– absorption in isolated sheep rumen mucosa. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 161, 419–426.
Short-chain fatty acids and CO2 as regulators of Na+ and Cl absorption in isolated sheep rumen mucosa.Crossref | GoogleScholarGoogle Scholar | 1939746PubMed |

Gaebel G, Bell M, Martens H (1989) The effect of low mucosal pH on sodium and chloride movement across the isolaged rumen mucosa of sheep. Quarterly Journal of Experimental Physiology 74, 35–44.

Gozho GN, Krause DO, Plaizier JC (2006) Rumen lipopolysaccharide and inflammation during grain adaptation and subacute ruminal acidosis in steers. Journal of Dairy Science 89, 4404–4413.
Rumen lipopolysaccharide and inflammation during grain adaptation and subacute ruminal acidosis in steers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtFens7%2FF&md5=5187aeac395301c3dc5ab0f4e17d7decCAS | 17033028PubMed |

Jutfelt F (2013) ‘Barrier function of the gut.’ (University of Gothenberg: Gothenberg, Sweden)

Farrel A (Ed.) (Year) ‘Encylopedia of fish physiology, from genome to environment.’ 1st edn. (Academic Press: Waltham, MA)

Mani V, Harris AJ, Keating AF, Weber TE, Dekkers JC, Gabler NK (2013) Intestinal integrity, endotoxin transport and detoxification in pigs divergently selected for residual feed intake. Journal of Animal Science 91, 2141–2150.
Intestinal integrity, endotoxin transport and detoxification in pigs divergently selected for residual feed intake.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXotl2gtrs%3D&md5=476ea38a659bd058e522e8d5390ac244CAS | 23463550PubMed |

Markov AG, Veshnyakova A, Fromm M, Amasheh M, Amasheh S (2010) Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine. Journal of Comparative Physiology. B, Biochemical, Systemic, and Environmental Physiology 180, 591–598.
Segmental expression of claudin proteins correlates with tight junction barrier properties in rat intestine.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXjtlGhsb0%3D&md5=73fa7b47235074926b4968ebe89e8226CAS | 20049600PubMed |

McKie AT, Zammit PS, Naftalin RJ (1999) Comparison of cattle and sheep colonic permeabilities to horseradish peroxidase and hamster scrapie prion protein in vitro. Gut 45, 879–888.
Comparison of cattle and sheep colonic permeabilities to horseradish peroxidase and hamster scrapie prion protein in vitro.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXhvV2jtA%3D%3D&md5=11a81e21cead807fe0d0326d95ff102eCAS | 10562587PubMed |

Nejdfors P, Ekelund M, Jeppsson B, Weström BR (2000) Mucosal in vitro permeability in the intestinal tract of the pig, the rat, and man: species- and region-related differences. Scandinavian Journal of Gastroenterology 35, 501–507.
Mucosal in vitro permeability in the intestinal tract of the pig, the rat, and man: species- and region-related differences.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3cXktlWrtLg%3D&md5=3ef1cb9d29567b7e8a6e9c543ab1bbd0CAS | 10868453PubMed |

Nitta H, Sugawara T, Sugawara E, Kobayashi Y, Katoh K, Obara Y (2005) Absorption of horseradish peroxidase (HRP) in vitro across bovine jejunal and ileal epithelia around the time of weaning. Tohoku Journal of Agricultural Research 56, 1–10.

Novosad VL, Richards JL, Phillips NA, King MA, Clanton TL (2013) Regional susceptibility to stress-induced intestinal injury in the mouse. American Journal of Physiology. Gastrointestinal and Liver Physiology 305, G418–G426.
Regional susceptibility to stress-induced intestinal injury in the mouse.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Sqsb3F&md5=c0454ed859234071eeb2ce6d9f85bebdCAS | 23868412PubMed |

Penner GB, Oba M, Gabel G, Aschenbach JR (2010) A single mild episode of subacute ruminal acidosis does not affect ruminal barrier function in the short term. Journal of Dairy Science 93, 4838–4845.
A single mild episode of subacute ruminal acidosis does not affect ruminal barrier function in the short term.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsFKmsLfK&md5=191437d28e6208ad9abcba3c2963dedfCAS | 20855017PubMed |

Presnell KR, Roe WE, Nielsen NO, Hamilton DL (1979) Permeability properties of swine small intestine: effect of a heat stable Escherichia coli enterotoxin. Canadian Journal of Comparative Medicine 43, 44–49.

Rupp GP (1994) Measurement of volatile fatty acid disappearance and fluid flux across the abomasum of cattle, using an improve omasal cannulation technique. American Journal of Veterinary Research 55, 522–529.

Sehested J, Diernæs L, Møller PD, Skadhauge E (1999) Ruminal transport and metabolism of short-chain fatty acids (SCFA) in vitro: effect of SCFA chain length and pH. Comparative Biochemistry and Physiology Part A 123, 359–368.
Ruminal transport and metabolism of short-chain fatty acids (SCFA) in vitro: effect of SCFA chain length and pH.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BD3c%2FkvVCjsA%3D%3D&md5=b2e4b8898c0fcbba04f81fc6f7b1ba7cCAS |

Vojdani A (2013) For the assessment of intestinal permeability, size matters. The Journal of Alternative Therapies 19, 12–24.

Wang Q, Pantzar N, Jeppsson B, Weström BR, Karlsson BW (1994) Increased intestinal marker absorption due to regional permeability changes and decreased intestinal transit during sepsis in the rat. Scandinavian Journal of Gastroenterology 29, 1001–1008.
Increased intestinal marker absorption due to regional permeability changes and decreased intestinal transit during sepsis in the rat.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DyaK2M7ns1WlsA%3D%3D&md5=0a7a86dae5a06626858febfa7ab84de2CAS | 7871365PubMed |

Wilkens MR, Mrochen N, Breves G, Schröder B (2011) Gastrointestinal calcium absorption in sheep is mostly insensitive to an alimentary induced challenge of calcium homeostasis. Comparative Biochemistry and Physiology. B, Comparative Biochemistry 158, 199–207.
Gastrointestinal calcium absorption in sheep is mostly insensitive to an alimentary induced challenge of calcium homeostasis.Crossref | GoogleScholarGoogle Scholar |

Wilson DJ, Mutsvangwa T, Penner GB (2012) Supplemental butyrate does not enhance the absorptive or barrier functions of the isolated ovine ruminal epithelia. Journal of Animal Science 90, 3153–3161.
Supplemental butyrate does not enhance the absorptive or barrier functions of the isolated ovine ruminal epithelia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38XhsVKku7nI&md5=00fd4a13f18a62680e83ab144de8d206CAS | 22585785PubMed |

Zhang S, Albornoz RI, Aschenbach JR, Barreda DR, Penner GB (2013a) Short-term feed restriction impairs the absorptive function of the reticulo-rumen and total tract barrier function in beef cattle. Journal of Animal Science 91, 1685–1695.
Short-term feed restriction impairs the absorptive function of the reticulo-rumen and total tract barrier function in beef cattle.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWrtbg%3D&md5=693ac6c0f5f4535ef47148919eb1d150CAS | 23422009PubMed |

Zhang S, Aschenbach JR, Barreda DR, Penner GB (2013b) Recovery of absorptive function of the reticulo-rumen and total tract barrier function in beef cattle after short-term feed restriction. Journal of Animal Science 91, 1696–1706.
Recovery of absorptive function of the reticulo-rumen and total tract barrier function in beef cattle after short-term feed restriction.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXntFWrtbk%3D&md5=3dc77a1038f0eeb8e8140c334ade9583CAS | 23408814PubMed |