Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

The effect of pre- and probiotics on the colonic ammonia metabolism in humans as measured by lactose-[15N2]ureide

Abstract

Background:

The evaluation of ammonia detoxification by pre- and probiotics by means of colonic lactose-[15N2]ureide (15N-LU) degradation is of great interest both scientifically and in terms of nutrition physiology.

Objective:

Pre- and probiotics were supplemented in healthy adults to evaluate the effect of the ammonia metabolism in the human colon by means of 15N-LU.

Methods:

A total of 14 participants aged 20–28 years daily received a regular diet either without (no treatment) or with supplementation of 30 g fibre of potatoes (FPs), 30 g wrinkle pea starch (WPS, resistant starch content: 12 and 70%, respectively) and 375 g Lactobacillus acidophilus (LC1) yoghurt, over a 10-day period in a randomised order. After 1 week, 5.7 mg/kg body weight 15N-LU was administered together with breakfast. A venous blood sample was taken after 6 h. Urine and faeces were collected over a period of 48 and 72 h, respectively. The 15N abundances were measured by isotope ratio mass spectrometry.

Results:

The mean renal 15N-excretion differed significantly between the supplementation of FP and no treatment (32.5 versus 46.3%, P=0.034), FP and LC1 (32.5 versus 51.6%, P=0.001), and WPS and LC1 (38.5 versus 51.6%, P=0.048). The mean faecal 15N-excretion amounted to 42.7% (no treatment), 59.7% (FP), 41.8% (WPS) and 44.0% (LC1). In comparison with no treatment, the urinary 15NH3-enrichment was significantly decreased at 16 h after FP supplementation.

Conclusion:

The prebiotic intake of FP and WPS lowered the colonic generation and the renal excretion of toxic 15NH3, respectively, when using 15N-LU as a xenobiotic marker.

This is a preview of subscription content, access via your institution

Access options

Buy article

Get time limited or full article access on ReadCube.

$32.00

All prices are NET prices.

Figure 1
Figure 2

References

  • Birkett A, Muir J, Phillips J, Jones G, O’Dea K (1996). Resistant starch lowers fecal concentrations of ammonia and phenols in humans. Am J Clin Nutr 63, 766–772.

    Article  CAS  PubMed  Google Scholar 

  • Cummings JH, Macfarlane GT (2002). Gastrointestinal effects of prebiotics. Br J Nutr 87 (Suppl 2), 145–151.

    Article  Google Scholar 

  • Cloetens L, De Preter V, De Loor H, Rutgeerts P, Verbeke K (2008a). Does the biomarker 15N-lactose ureide allow to estimate the site of fermentation of resistant starch. Eur J Nutr 47, 217–223.

    Article  CAS  PubMed  Google Scholar 

  • Cloetens L, De Preter V, Swennen K, Broekaert WF, Courtin CM, Delcour JA et al. (2008b). Dose-response effect of arabinoxylooligosaccharides on gastrointestinal motility and on colonic bacterial metabolism in healthy volunteers. J Am Coll Nutr 27, 512–518.

    Article  CAS  PubMed  Google Scholar 

  • De Preter V, Geboes K, Verbrugghe K, De Vuyst L, Vanhoutte T, Huys G et al. (2004). The in vivo use of the stable isotope-labelled biomarkers lactose-[15N]ureide and [2H4]tyrosine to assess the effects of pro- and prebiotics on the intestinal flora of healthy human volunteers. Br J Nutr 92, 439–446.

    Article  CAS  PubMed  Google Scholar 

  • De Preter V, Verbeke K (2006). Evaluation of the necessity of induction for lactose-[15N,15N]-ureide to study the colonic ammonia metabolism. Scand J Gastroenterol 41, 396–400.

    Article  CAS  PubMed  Google Scholar 

  • De Preter V, Vanhoutte T, Huys G, Swings J, De Vuyst L, Rutgeerts P et al. (2007). Effects of Lactobacillus casei Shirota, Bifidobacterium breve, and oligofructose-enriched inulin on colonic nitrogen-protein metabolism in healthy humans. Am J Physiol Gastroenterol Liver Physiol 292, G358–G368.

    Article  CAS  Google Scholar 

  • De Preter V, Vanhoutte T, Huys G, Swings J, Rutgeerts P, Verbeke K (2006). Effect of lactulose and Saccharomyces boulardii administration on the colonic urea-nitrogen metabolism and the bifidobacteria concentration in healthy human subjects. Aliment Pharmacol Ther 23, 963–974.

    Article  CAS  PubMed  Google Scholar 

  • De Preter V, Vanhoutte T, Huys G, Swings J, Rutgeerts P, Verbeke K (2008). Baseline microbiota activity and initial bifidobacteria counts influence responses to prebiotic dosing in healthy subjects. Aliment Pharmacol Ther 27, 504–513.

    Article  CAS  PubMed  Google Scholar 

  • Faust H, Bornhak H, Hirschberg K, Jung K, Junghans P, Krumbiegel P et al. (1981). Klinisch-chemische und isotopenanalytische Methoden zur Untersuchung des Stickstoff-Stoffwechsels mit N-15 beim Menschen. In: Wetzel K (ed). Methodenkatalog. ZfI-Mitteilungen. vol. 36 Akademie der Wissenschaften: Leipzig. pp 115–132.

    Google Scholar 

  • Fuller R (1989). Probiotics in man and animals. J Appl Bacteriol 66, 365–378.

    Article  CAS  PubMed  Google Scholar 

  • Geboes KP, De Hertogh G, De Preter V, Luypaerts A, Bammens B, Evenepoel P et al. (2006). The influence of inulin on the absorption of nitrogen and the production of metabolites of protein fermentation in the colon. Br J Nutr 96, 1078–1086.

    Article  CAS  PubMed  Google Scholar 

  • Geboes KP, De Preter V, Luypaerts A, Bammens B, Evenepoel P, Ghoos Y et al. (2005). Validation of lactose[15N,15N]ureide as a tool to study colonic nitrogen metabolism. Am J Physiol Gastrointest Liver Physiol 288, G994–G999.

    Article  CAS  PubMed  Google Scholar 

  • Gibson GR, Roberfroid MB (1995). Dietary modulation of the human colonic microbiota: introducing the concept of prebiotics. J Nutr 125, 1401–1412.

    Article  CAS  PubMed  Google Scholar 

  • Heijnen ML, Beynen AC (1997). Consumption of retrograded (RS3) but not uncooked (RS2) resistant starch shifts nitrogen excretion from urine to feces in cannulated piglets. J Nutr 127, 1828–1832.

    Article  CAS  PubMed  Google Scholar 

  • Heine WE, Berthold HK, Klein PD (1995). A novel stable isotope breath test: 13C-labeled glycosylureides used as noninvasive markers of intestinal transit time. Am J Gastroenterol 90, 93–98.

    CAS  PubMed  Google Scholar 

  • Jackson AA, Gibson NR, Bundy R, Hounslow A, Millward DJ, Wootton SA (2004). Transfer of 15N from oral lactose-ureide to lysine in normal adults. Int J Food Sci Nutr 55, 455–462.

    Article  CAS  PubMed  Google Scholar 

  • Macfarlane GT, Cummings JH (1991). The colonic flora, fermentation and large bowel digestive function. In: Phillips SF, Pemberton H, Shorter RG (eds). The Large Intestine: Physiology, Pathophysiology and Disease. Raven: New York. pp 51–92.

    Google Scholar 

  • Mohr C, Heine WE, Wutzke KD (1999). Clostridium innocuum: a glucose ureide splitting inhabitant of the human microbial flora. Biochim Biophys Acta 1472, 550–554.

    Article  CAS  PubMed  Google Scholar 

  • Pfeiffer A, Rosat JP (1999). Probiotics in alimentation: clinical evidence for their enhancement of the natural immunity of the gut. In: Hanson LA, Yolken RH (eds). Probiotics, Other Nutritional Factors and Intestinal Microflora. Nestlé nutrition workshop series. vol. 42 Lippincott-Raven: Philadelphia. pp 243–255.

    Google Scholar 

  • Sajilata MG, Singhal RS, Kulkarni PR (2006). Resistant starch—a review. Compr Rev Food Sci Food Saf 5, 1–17.

    Article  CAS  PubMed  Google Scholar 

  • Sanders MA, Huis In’t Veld J (1999). Bringing a probiotic-containing functional food on the market: microbiological, product, regulatory and labeling issues. Antonie Van Leeuwenhoek 76, 293–315.

    Article  CAS  PubMed  Google Scholar 

  • Smith EA, Macfarlane GT (1996). Enumeration of human colonic bacteria producing phenolic and indolic compounds: effects of pH, carbohydrate availability and retention time on dissimilatory aromatic amino acid metabolism. J Appl Bacteriol 81, 288–302.

    Article  CAS  PubMed  Google Scholar 

  • Swanson KS, Grieshop CM, Flickinger EA, Bauer LL, Chow J, Wolf BW et al. (2002). Fructooligosaccharides and Lactobacillus acidophilus modify gut microbial populations, total tract nutrient digestibilities and fecal protein catabolite concentrations in healthy adult dogs. J Nutr 132, 3721–3731.

    Article  CAS  PubMed  Google Scholar 

  • Wutzke KD, Glasenapp B (2004). The use of 13C-labelled glycosyl ureides for evaluation of orocaecal transit time. Eur J Clin Nutr 58, 568–572.

    Article  CAS  PubMed  Google Scholar 

  • Wutzke KD, Heine WE, Plath C, Leitzmann P, Radke M, Mohr C et al. (1997). Evaluation of oro-coecal transit time: a comparison of the lactose-[13C, 15N]ureide 13CO2- and the lactulose H2-breath test in humans. Eur J Clin Nutr 51, 11–19.

    Article  CAS  PubMed  Google Scholar 

  • Wutzke KD, Oetjens I (2005). 13C- and 15N-incorporation of doubly stable isotope labelled Lactobacillus johnsonii in humans. Eur J Clin Nutr 59, 1167–1172.

    Article  CAS  PubMed  Google Scholar 

  • Wutzke KD, Sattinger V (2006). 15N-excretion of heat-killed Lactobacillus casei in humans. Eur J Clin Nutr 60, 847–852.

    Article  CAS  PubMed  Google Scholar 

  • Wutzke KD, Schütt M (2007). The duration of enzyme induction in oroceacal transit time measuremenrts. Eur J Clin Nutr 61, 1161–1166.

    Article  Google Scholar 

Download references

Acknowledgements

This study was supported by Emsland Group GmbH Emlichheim, Germany.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to K D Wutzke.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Wutzke, K., Lotz, M. & Zipprich, C. The effect of pre- and probiotics on the colonic ammonia metabolism in humans as measured by lactose-[15N2]ureide. Eur J Clin Nutr 64, 1215–1221 (2010). https://doi.org/10.1038/ejcn.2010.120

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/ejcn.2010.120

Keywords

  • ammonia metabolism
  • human colon
  • lactose-[15N2]ureide
  • prebiotics
  • probiotics

This article is cited by

Search

Quick links