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13C- and 15N-incorporation of doubly stable isotope labelled Lactobacillus johnsonii in humans

Abstract

Objective:

In the present study, Lactobacillus johnsonii (La1) doubly labelled with 15N and 13C (dlLa1) was used to follow the metabolic fate of orally administered dlLa1 in humans.

Design:

Experimental study.

Setting:

Research Laboratory, Children's Hospital, University of Rostock.

Subjects:

A total of 10 healthy adults aged 23–36 y.

Intervention:

The subjects received 87 mg/kg body weight viable dlLa1 and 10 g raffinose together with breakfast. Expired air samples were taken over 14 h, whereas urine and faeces were collected over 2 days. A blood sample was taken after 2 h. 13C- and 15N-enrichments were measured by isotope ratio mass spectrometry (SerCon, UK) and H2-concentrations were measured by electrochemical detection (Stimotron, Germany).

Results:

The orocaecal transit time (OCTT) was reached after 3.7 h. The 13CO2-exhalation amounted to 8.6% of ingested dose. The urinary excretion of 13C and 15N was 1.3 and 12.4% of ingested dose, respectively, whereas the faecal excretion was 39.9 and 37.6% of ingested dose, respectively. After 2 h, 13C- and 15N-enrichment of fibrinogen amounted to 70 and 90 ppm excess, respectively.

Conclusions:

In comparison to OCTT of 3.7 h, both stable isotopes appear after 30 min in breath and urine, indicating that dlLa1 is rapidly digested in the small bowel before reaching the caecum. This is confirmed by 13C-and 15N-enrichments of blood plasma fractions. The ingestion of dlLa1 led to an excretion of 50% of ingested dose of both stable isotopes.

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References

  • Alm L (1989): The therapeutic effects of various cultures – an overview. In Therapeutic Properties of Fermented Milks ed RK Robinson New York: Elsevier Applied Science.

    Google Scholar 

  • Barrie A, Davies JE, Park AJ & Workmann CT (1989): Continuous-flow stable isotope analysis for biologists. Spectroscopy 4, 42–52.

    CAS  Google Scholar 

  • Bernet MF, Brassat D, Neeser JR & Serving AL (1994): Lactobacillus acidophilus La1 binds to cultured human intestinal cell lines and inhibits cell attachment and cell invasion by enterovirulent bacteria. Gut 35, 483–489.

    Article  CAS  Google Scholar 

  • Brösicke H (1987): Bestimmung der Fettsäureoxidation Frühgeborener mit dem 13CO2 Atemtest während kontinuierlicher 13C-Triolein-Infusion. In Klinische Ernährung eds FW Ahnefeld, W Hartig, E Holm & G Kleinberger, pp 4–17. München, Bern, Wien, San Francisco: Zuckschwerdt.

    Google Scholar 

  • Coplen TB (1996): New guidelines for reporting stable hydrogen, carbon, and oxygen isotope-ratio data. Geochim. Cosmochim. Acta 60, 3359–3360.

    Article  CAS  Google Scholar 

  • De Man JD, Rogosa M & Sharpe ME (1960): A Medium for the cultivation of Lactobacilli. J. Appl. Bacteriol. 23, 130–135.

    Article  Google Scholar 

  • Faust H, Bornhak H, Hirschberg K, Jung K, Junghans P, Krumbiegel P & Reinhardt R (1981): Klinisch-chemische und isotopenanalytische Methoden zur Untersuchung des Stickstoff-Stoffwechsels mit N-15 beim Menschen. Methodenkatalog pp 1–210. Leipzig: Akademie der Wissenschaften.

    Google Scholar 

  • Finegold SM, Sutter VL & Mathisen GE (1983): Normal indigenous intestinal flora. In Human Intestinal Flora in Health and Disease ed DJ Hentges, pp 3–31. New York: Academic Press.

    Chapter  Google Scholar 

  • Fioramonti J, Theodorou V & Bueno L (2003): Probiotics: what are they? What are their effects on gut physiology? Best Pract. Res. Clin. Gastroenterol. 17, 711–724.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Haycock GB, Schwartz GJ & Wisotzki DH (1978): Geometric method for measuring body surface area: a hight-weight formula validated in infants, children and adults. J. Pediatr. 93, 62–66.

    Article  CAS  Google Scholar 

  • Heine WE, Mohr C & Wutzke KD (1992): Host-microflora correlations in infant nutrition. Prog. Food Nutr. Sci. 16, 181–197.

    CAS  PubMed  Google Scholar 

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

    CAS  Google Scholar 

  • Heine W, Mohr C & Münch C (1996): Zuckerverbindungen als Substrate für Wasserstoff-Atemgasteste: Korreleation zur Dosis, orozökalen Transitzeit, Mikroflora und zu Nebenwirkungen. Pädiatr. Grenzgeb. 34, 481–490.

    Google Scholar 

  • Kandler O & Weiss N (1986): Genus Lactobacillus. In Bergey's Manual of Systematic Bacteriology, Vol. II eds PHA Sneath, NS Mair, ME Sharpe & JG Holt Baltimore: Williams & Wilkins.

    Google Scholar 

  • Kimoto H, Nomura M, Kobayashi M, Mizumachi K & Okamoto T (2003): Survival of lactococci during passage through mouse digestive tract. Can. J. Microbiol. 49, 707–711.

    Article  CAS  Google Scholar 

  • King CE & Toskes PP (1986): Comparison of the 1-gram [14C]xylose, 10-gram lactulose-H2, and 80-gram glucose-H2 breath test in patients with small intestine bacterial overgrowth. Gastroenterology 91, 1447–1451.

    Article  CAS  Google Scholar 

  • Lee YK & Salminen S (1995): The coming age of probiotics. Trends Food Sci. Technol. 6, 241–245.

    Article  Google Scholar 

  • Leitzmann P, Heine W, Wutzke KD, von Bismarck P, Dorlöchter L, Miera O, Bührlen M, Corneließen BW & Höcker C (1998): Blood glucose, gastric emptying, and oro-coecal transit time after a conventional breakfast vs. a Kollath breakfast. Z. Ernährungswiss. 37, 31–37.

    Article  CAS  Google Scholar 

  • Meydani SN & Ha WK (2000): Immunologic effects of yogurt. Am. J. Clin. Nutr. 71, 861–872.

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Radke M, Heine W, Wutzke KD, Leitzmann P & Walther F (1995): Tracer kinetic studies on a methionine-supplemented soy-based infant formula using 1-13C- and 15N-methionine as tracers. J. Pediatr. Gastroenterol. Nutr. 21, 209–214.

    Article  CAS  Google Scholar 

  • Robins-Browne RM & Levine MM (1981): The fate of ingested lactobacilli in the proximal small intestine. Am. J. Clin. Nutr. 34, 514–519.

    Article  CAS  Google Scholar 

  • Sarno S, Erasmus LP, Haslbeck M & Holzl R (1993): Orocaecal transit-time by the H2 method: effects of definitions of caecal entry and test meal. Ital. J. Gastroenterol. 25, 55–64.

    CAS  PubMed  Google Scholar 

  • Schoeller DA, Klein PD, Watkins JB, Heim T & MacLean Jr WC (1980): 13C abundances of nutrients and the effect of variations in 13C isotopic abundances of test meals formulated for 13CO2 breath tests. Am. J. Clin. Nutr. 33, 2375–2385.

    Article  CAS  Google Scholar 

  • Slater C, Preston T & Weaver LT (2001): Stable isotopes and the international system of units. Rapid Commun. Mass Spectrom. 15, 1270–1273.

    Article  CAS  Google Scholar 

  • Vantrappen GR, Rutgeerts PJ, Ghoos YF & Hiele MI (1989): Mixed triglyceride breath test: a noninvasive test of pancreatic lipase activity in the duodenum. Gastroenterology 96, 1126–1134.

    Article  CAS  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  Google Scholar 

  • Wutzke KD, Heine W, Drescher U, Richter I & Plath C (1983): 15N-labelled yeast protein – a valid tracer for calculating whole-body protein parameters in infants: a comparison between [15N]-yeast protein and [15N]-glycine. Hum. Nutr. Clin. Nutr. 37C, 317–327.

    CAS  Google Scholar 

  • Wutzke KD, Heine W, Völker T, Kreyenbrink F & Krawielitzki K (1984): Präparative Darstellung von hochangereichertem 15N-markiertem Hefeprotein. Isotopenpraxis 20, 90–93.

    CAS  Google Scholar 

  • Wutzke KD, Heine W, Plath C, Müller M & Uhlemann M (1992): Whole-body protein parameters in premature infants: a comparison of different 15N tracer substances and different methods. Pediatr. Res. 31, 95–101.

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Wutzke KD, Heine WE, Köster D, Muscheites J, Mix M, Mohr C & Wigger M (2001): Metabolic effects of Hay’ diet. Isotopes Environ. Health Stud. 37, 227–237.

    Article  CAS  Google Scholar 

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Correspondence to K D Wutzke.

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Guarantor: KD Wutzke.

Contributor: IO was principal investigator and doctoral candidate of KDW.

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Wutzke, K., Oetjens, I. 13C- and 15N-incorporation of doubly stable isotope labelled Lactobacillus johnsonii in humans. Eur J Clin Nutr 59, 1167–1172 (2005). https://doi.org/10.1038/sj.ejcn.1602227

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  • DOI: https://doi.org/10.1038/sj.ejcn.1602227

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