Abstract
In ruminants, gastrointestinal recycling of urea is acutely enhanced by fibre-rich diets that lead to high ruminal concentration of short chain fatty acids (SCFA), while high ammonia has inhibitory effects. This study attempted to clarify if urea flux to the porcine cecum is similarly regulated. Thirty-two weaned piglets were fed diets containing protein (P) of poor prececal digestibility and fibre (F) at high (H) or low levels (L) in a 2 × 2 factorial design. After slaughter, cecal content was analyzed and the cecal mucosa incubated in Ussing chambers to measure the effect of pH, SCFA and NH4 + on the flux rates of urea, short-circuit current (I sc) and tissue conductance (G t). NH4 + significantly enhanced I sc (from 0.5 ± 0.2 to 1.2 ± 0.1 μEq cm−2 h−1). No acute effects of SCFA or ammonia on urea flux were observed. Tissue conductance was significantly lower in the high dietary fibre groups irrespective of the protein content. Only the HP-LF group emerged as different from all others in terms of urea flux (74 ± 6 versus 53 ± 3 nmol cm−2 h−1), associated with higher cecal ammonia concentration and reduced fecal consistency. The data suggest that as in the rumen, uptake of ammonia by the cecum may involve electrogenic transport of the ionic form (NH4 +). In contrast to findings in the rumen, neither a high fibre diet nor acute addition of SCFA enhanced urea transport across the pig cecum. Instead, a HP-LF diet had stimulatory effects. A potential role for urea recycling in stabilizing luminal pH is discussed.
Similar content being viewed by others
References
Abdoun K, Stumpff F, Wolf K, Martens H (2005) Modulation of electroneutral Na transport in sheep rumen epithelium by luminal ammonia. Am J Physiol 289(3):G508–G520
Abdoun K, Stumpff F, Martens H (2006) Ammonia and urea transport across the rumen epithelium: a review. Anim Health Res Rev 7(1–2):43–59
Abdoun K, Stumpff F, Rabbani I, Martens H (2010) Modulation of urea transport across sheep rumen epithelium in vitro by SCFA and CO2. Am J Physiol 298(2):G190–G202
Als-Nielsen B, Gluud LL, Gluud C (2004) Non-absorbable disaccharides for hepatic encephalopathy: systematic review of randomised trials. BMJ 328(7447):1046. doi:10.1136/bmj.38048.506134.EE
Backes G, Hennig U, Petzke KJ, Elsner A, Junghans P, Nurnberg G, Metges CC (2002) Contribution of intestinal microbial lysine to lysine homeostasis is reduced in minipigs fed a wheat gluten-based diet. Am J Clin Nutr 76(6):1317–1325
Bagnasco SM (2005) Role and regulation of urea transporters. Pflugers Arch 450(4):217–226
Baldwin RLt, Wu S, Li W, Li C, Bequette BJ, Li RW (2012) Quantification of transcriptome responses of the rumen epithelium to butyrate infusion using RNA-seq technology. Gene Regul Syst Biol 6:67–80. doi:10.4137/GRSB.S9687
Bergen WG, Wu G (2009) Intestinal nitrogen recycling and utilization in health and disease. J Nutr 139(5):821–825. doi:10.3945/jn.109.104497
Bergner H, Simon O, Zebrowska T, Munchmeyer R (1986) Studies on the secretion of amino acids and of urea into the gastrointestinal tract of pigs: 3. Secretion of urea determined by continuous intravenous infusion of 15N-urea. Arch Tierernahr 36(6):479–490
Bödeker D, Kemkowski J (1996) Participation of NH4 + in total ammonia absorption across the rumen epithelium of sheep (Ovis aries). Comp Biochem Physiol A Physiol 114(4):305–310
Darragh AJ, Cranwell PD, Moughan PJ (1994) Absorption of lysine and methionine from the proximal colon of the piglet. Br J Nutr 71(5):739–752. [pii: S0007114594000802]
Demigne C, Remesy C (1985) Stimulation of absorption of volatile fatty acids and minerals in the cecum of rats adapted to a very high fiber diet. J Nutr 115(1):53–60
Diener M, Scharrer E (1995) Swelling-activated conductances for chloride, potassium and amino acids in the rat colon: a whole-cell study. Exp Physiol 80(3):411–428
Dobson A, Sellers AF, Thorlacius SO (1971) Limitation of diffusion by blood flow through bovine ruminal epithelium. Am J Physiol 220(5):1337–1343
Doranalli K, Penner GB, Mutsvangwa T (2011) Feeding oscillating dietary crude protein concentrations increases nitrogen utilization in growing lambs and this response is partly attributable to increased urea transfer to the rumen. J Nutr 141(4):560–567. doi:10.3945/jn.110.133876
von Engelhardt W, Dycker C, Lechner-Doll M (2007) Absorption of short-chain fatty acids, sodium and water from the forestomach of camels. J Comp Physiol (B) 177(6):631–640
Fouillet H, Juillet B, Bos C, Mariotti F, Gaudichon C, Benamouzig R, Tome D (2008) Urea-nitrogen production and salvage are modulated by protein intake in fed humans: results of an oral stable-isotope-tracer protocol and compartmental modeling. Am J Clin Nutr 87(6):1702–1714. [pii: 87/6/1702]
Fuller MF, Reeds PJ (1998) Nitrogen cycling in the gut. Annu Rev Nutr 18:385–411. doi:10.1146/annurev.nutr.18.1.385
Gargallo J, Zimmerman D (1981a) Effect of casein and starch infusion in the large intestine on nitrogen metabolism of growing swine. J Nutr 111(8):1390–1396
Gargallo J, Zimmerman DR (1981b) Effects of dietary cellulose levels on intact and cecectomize pigs. J Anim Sci 53:395–402
Gärtner K, Decker P, Hill H (1961) Untersuchungen über die Passage von Harnstoff und Ammoniak durch die Pansenwand von Ziegen. Pflugers Arch 274:281–288
Harmeyer J, Martens H (1980) Aspects of urea metabolism in ruminants with reference to the goat. J Dairy Sci 63(10):1707–1728
Hume ID, Karasov WH, Darken BW (1993) Acetate, butyrate and proline uptake in the caecum and colon of prairie voles (Microtus ochrogaster). J Exp Biol 176:285–297
Just A, Jorgensen H, Fernandez JA (1981) The digestive capacity of the caecum-colon and the value of the nitrogen absorbed from the hind gut for protein synthesis in pigs. Br J Nutr 46(1):209–219. [pii: S0007114581000986]
Kennedy PM, Milligan LP (1978) Transfer of urea from the blood to the rumen of sheep. Br J Nutr 40(1):149–154
Leonhard-Marek S, Stumpff F, Brinkmann I, Breves G, Martens H (2005) Basolateral Mg2+/Na+ exchange regulates apical nonselective cation channel in sheep rumen epithelium via cytosolic Mg2+. Am J Physiol 288(4):G630–G645
LeVeen EG, Falk G, Ip M, Mazzapica N, LeVeen HH (1978) Urease as a contributing factor in ulcerative lesions of the colon. Am J Surg 135(1):53–56. [pii: 0002-9610(78)90009-0]
Mariadason JM, Catto-Smith A, Gibson PR (1999) Modulation of distal colonic epithelial barrier function by dietary fibre in normal rats. Gut 44(3):394–399
Marini J, Sands J, Van Amburgh M (2006) Urea transporters and urea recycling in ruminants. In: Sejrsen K, Hvelplund T, Nielsen M (eds) Ruminant physiology. Wageningen Academic Publishers, Wageningen, pp 155–171
Metges CC, Petzke KJ, El-Khoury AE, Henneman L, Grant I, Bedri S, Regan MM, Fuller MF, Young VR (1999) Incorporation of urea and ammonia nitrogen into ileal and fecal microbial proteins and plasma free amino acids in normal men and ileostomates. Am J Clin Nutr 70(6):1046–1058
Mosenthin R, Sauer WC, de Lange CF (1992a) Tracer studies of urea kinetics in growing pigs: I. The effect of intravenous infusion of urea on urea recycling and the site of urea secretion into the gastrointestinal tract. J Anim Sci 70(11):3458–3466
Mosenthin R, Sauer WC, Henkel H, Ahrens F, de Lange CF (1992b) Tracer studies of urea kinetics in growing pigs: II. The effect of starch infusion at the distal ileum on urea recycling and bacterial nitrogen excretion. J Anim Sci 70(11):3467–3472
Pastuszewska B, Kowalczyk J, Ochtabinska A (2000) Dietary carbohydrates affect caecal fermentation and modify nitrogen excretion patterns in rats. II. Studies with diets differing in protein quality. Arch Tierernahr 53(4):335–352
Peng L, Li ZR, Green RS, Holzman IR, Lin J (2009) Butyrate enhances the intestinal barrier by facilitating tight junction assembly via activation of AMP-activated protein kinase in Caco-2 cell monolayers. J Nutr 139(9):1619–1625. doi:10.3945/jn.109.104638
Pieper R, Kroger S, Richter JF, Wang J, Martin L, Bindelle J, Htoo JK, von Smolinski D, Vahjen W, Zentek J, Van Kessel AG (2012) Fermentable fiber ameliorates fermentable protein-induced changes in microbial ecology, but not the mucosal response, in the colon of piglets. J Nutr 142(4):661–667. doi:10.3945/jn.111.156190
Ploger S, Stumpff F, Penner GB, Schulzke JD, Gabel G, Martens H, Shen Z, Gunzel D, Aschenbach JR (2012) Microbial butyrate and its role for barrier function in the gastrointestinal tract. Ann NY Acad Sci 1258:52–59. doi:10.1111/j.1749-6632.2012.06553.x
Remesy C, Demigne C (1989) Specific effects of fermentable carbohydrates on blood urea flux and ammonia absorption in the rat cecum. J Nutr 119(4):560–565
Remond D, Chaise JP, Delval E, Poncet C (1993) Net transfer of urea and ammonia across the ruminal wall of sheep. J Anim Sci 71(10):2785–2792
Remond D, Noziere P, Poncet C (2002) Effect of time of starch supply to the rumen on the dynamics of urea and ammonia net flux across the rumen wall of sheep. Anim Res 51:3–13
Reynolds CK, Huntington GB (1988) Partition of portal-drained visceral net flux in beef steers. 1. Blood flow and net flux of oxygen, glucose and nitrogenous compounds across stomach and post-stomach tissues. Br J Nutr 60(3):539–551
Reynolds CK, Kristensen NB (2008) Nitrogen recycling through the gut and the nitrogen economy of ruminants: an asynchronous symbiosis. J Anim Sci 86(14 Suppl):E293–E305
Ross MH, Romrell LJ, Kaye GI (1995) Histology: a text and atlas, 3rd edn. Williams and Wilkins, Baltimore
Roy CC, Kien CL, Bouthillier L, Levy E (2006) Short-chain fatty acids: ready for prime time? Nutr Clin Pract 21(4):351–366
Satter LD, Slyter LL (1974) Effect of ammonia concentration of rumen microbial protein production in vitro. Br J Nutr 32(2):199–208
Sellin JH, Dubinsky WP (1994) Apical nonspecific cation conductances in rabbit cecum. Am J Physiol 266(3 Pt 1):G475–G484
Souffrant WB, Rerat A, Laplace JP, Darcy-Vrillon B, Kohler R, Corring T, Gebhardt G (1993) Exogenous and endogenous contributions to nitrogen fluxes in the digestive tract of pigs fed a casein diet. III. Recycling of endogenous nitrogen. Reprod Nutr Dev 33(4):373–382
Stevens CE, Hume ID (1998) Contributions of microbes in vertebrate gastrointestinal tract to production and conservation of nutrients. Physiol Rev 78(2):393–427
Stumpff F, Martens H, Bilk S, Aschenbach JR, Gabel G (2009) Cultured ruminal epithelial cells express a large-conductance channel permeable to chloride, bicarbonate, and acetate. Pflugers Archiv (European Journal of Physiology) 457(5):1003–1022. doi:10.1007/s00424-008-0566-6
Suzuki T, Yoshida S, Hara H (2008) Physiological concentrations of short-chain fatty acids immediately suppress colonic epithelial permeability. Br J Nutr 100(2):297–305. doi:10.1017/S0007114508888733
Thacker PA, Bowland JP, Milligan LP, Weltzien E (1982) Effects of graded dietary protein levels on urea recycling in the pig. Can J Anim Sci 62:1193–1197
Thorlacius SO, Dobson A, Sellers AF (1971) Effect of carbon dioxide on urea diffusion through bovine ruminal epithelium. Am J Physiol 220(1):162–170
Vaziri ND, Yuan J, Norris K (2012) Role of urea in intestinal barrier dysfunction and disruption of epithelial tight junction in chronic kidney disease. Am J Nephrol 37(1):1–6. doi:10.1159/000345969
Wickersham TA, Titgemeyer EC, Cochran RC, Wickersham EE, Gnad DP (2008) Effect of rumen-degradable intake protein supplementation on urea kinetics and microbial use of recycled urea in steers consuming low-quality forage. J Anim Sci 86(11):3079–3088
Xiao L, Xiao M, Jin X, Kawasaki K, Ohta N, Sakaguchi E (2012) Transfer of blood urea nitrogen to cecal microbial nitrogen is increased by mannitol feeding in growing rabbits fed timothy hay diet. Animal 6(11):1757–1763. doi:10.1017/S1751731112000754
Younes H, Garleb K, Behr S, Remesy C, Demigne C (1995) Fermentable fibers or oligosaccharides reduce urinary nitrogen excretion by increasing urea disposal in the rat cecum. J Nutr 125(4):1010–1016
Younes H, Remesy C, Behr S, Demigne C (1997) Fermentable carbohydrate exerts a urea-lowering effect in normal and nephrectomized rats. Am J Physiol 272(3 Pt 1):G515–G521
Zervas S, Zijlstra RT (2002) Effects of dietary protein and fermentable fiber on nitrogen excretion patterns and plasma urea in grower pigs. J Anim Sci 80(12):3247–3256
Acknowledgments
We wish to thank Uwe Tietjen, Ujkan Ujkani, Driton Caushi, Zhongyan Lu, and Alexandra Otte for their skilful help during the experiments. The study was supported by Evonik Industries (Hanau–Wolfgang, Germany), the German Research Foundation through Grant No. SFB852/1, and the Canadian Swine Research and Development Cluster.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume.
Rights and permissions
About this article
Cite this article
Stumpff, F., Lodemann, U., Van Kessel, A.G. et al. Effects of dietary fibre and protein on urea transport across the cecal mucosa of piglets. J Comp Physiol B 183, 1053–1063 (2013). https://doi.org/10.1007/s00360-013-0771-2
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-013-0771-2