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Digestive Diseases and Sciences

, Volume 55, Issue 10, pp 2778–2784 | Cite as

Sucrose Co-administration Reduces the Toxic Effect of Lectin on Gut Permeability and Intestinal Bacterial Colonization

  • Balamurugan Ramadass
  • Karol Dokladny
  • Pope L. Moseley
  • Yatin R. Patel
  • Henry C. LinEmail author
Original Article

Abstract

Introduction

Legume lectins can have toxic effects when consumed without adequate cooking, occasionally leading to an acute gastroenteritis. Lectins are sugar binging proteins and may use this property to execute their toxic effects; these toxic effects may be secondary to increased gut bacteria and intestinal permeability. However, whether or not sucrose rescues these toxic effects by decreasing gut bacterial concentration and intestinal permeability is unknown.

Aim

Our aim was to test the hypothesis that sucrose may reduce toxic effects of legume lectins by protecting barrier function, bacterial overgrowth and bacterial translocation.

Methods

Twenty-four rats were randomized to an ad libitum diet of either standard rat chow, a chow containing 26% crude red kidney beans or a chow containing 26% crude red kidney beans supplemented with 1 mM sucrose in drinking water for 24 h. After 12-h fast, rats were gavaged with sugar probes; breath gas and urine were collected for 5 h. Intestine and liver tissues were then collected. Mucosa-associated total bacterial count were measured by targeting the 16s rRNA gene. Four groups of in vitro Caco-2 cell lines were treated with PBS, 200 μg/ml phytohemagglutinin (PHA), 1 mM sucrose and both 200 μg/ml PHA and 1 mM sucrose, respectively, and trans-epithelial resistance was measured.

Results

Rats fed crude red kidney beans for 24 h showed significant weight loss when compared to controls (P < 0.05), as well as increased intestinal permeability (P < 0.05), increased bacterial load (P < 0.05) and increased bacterial translocation to the liver (P < 0.05). Sucrose rescues the drop in trans-epithelial resistance due to PHA in CaCO2-cells (P < 0.05).

Conclusions

Sucrose reduced crude red kidney beans induced increase in intestinal permeability, bacterial load and translocation. Since red kidney beans are an important source of dietary protein in the world, their potential toxicity when inadequately cooked may be rescued by a suitable complementary diet.

Keywords

Sucrose rescue Bacterial overgrowth Intestinal permeability Bacterial translocation Crude red kidney beans 

Notes

Acknowledgments

The authors gratefully acknowledge Tori Thomas for supporting Dr. Ramadass’ postdoctoral fellowship.

Author contributions

The author’s roles were as follows—HCL, PLM and RB were responsible for conception, analysis of data, and writing the manuscript; KD, YRP and RB were responsible for animal experiments, sample and data collection, PCR analyses and histology. None of the authors had a personal or financial conflict of interest.

Funding

Dr. Lin’s research is supported by the NIH, the VA Research Office and the Department of Defense.

Competing interest

None to declare. Dr. Lin has intellectual property rights in the area of bacterial overgrowth.

References

  1. 1.
    Reyes-Moreno C, Paredes-Lopez O. Hard-to-cook phenomenon in common beans—a review. Crit Rev Food Sci Nutr. 1993;33(3):227–286.CrossRefPubMedGoogle Scholar
  2. 2.
    Mongeau R, Brassard R. Importance of cooking temperature and pancreatic amylase in determination of dietary fiber in dried legumes. J AOAC Int. 1995;78(6):1444–1449.PubMedGoogle Scholar
  3. 3.
    Paredes-Lopez O, Carabez-Trejo A, Palma-Tirado L, Reyes-Moreno C. Influence of hardening procedure and soaking solution on cooking quality of common beans. Plant Foods Hum Nutr. 1991;41(2):155–164.CrossRefPubMedGoogle Scholar
  4. 4.
    Cummings RD, Kornfeld S. Characterization of the structural determinants required for the high affinity interaction of asparagine-linked oligosaccharides with immobilized Phaseolus vulgaris leukoagglutinating and erythroagglutinating lectins. J Biol Chem. 1982;257(19):11230–11234.PubMedGoogle Scholar
  5. 5.
    Myer RO, Froseth JA, Coon CN. Protein utilization and toxic effects of raw beans (Phaseolus vulgaris) for young pigs. J Anim Sci. 1982;55(5):1087–1098.PubMedGoogle Scholar
  6. 6.
    Weinman MD, Allan CH, Trier JS, Hagen SJ. Repair of microvilli in the rat small intestine after damage with lectins contained in the red kidney bean. Gastroenterology. 1989;97(5):1193–1204.PubMedGoogle Scholar
  7. 7.
    Boldt DH, Banwell JG. Binding of isolectins from red kidney bean (Phaseolus vulgaris) to purified rat brush-border membranes. Biochim Biophys Acta. 1985;843(3):230–237.PubMedGoogle Scholar
  8. 8.
    Baintner K, Duncan SH, Stewart CS, Pusztai A. Binding and degradation of lectins by components of rumen liquor. J Appl Bacteriol. 1993;74(1):29–35.PubMedGoogle Scholar
  9. 9.
    Noah ND, Bender AE, Reaidi GB, Gilbert RJ. Food poisoning from raw red kidney beans. Br Med J. 1980;281(6234):236–237.PubMedGoogle Scholar
  10. 10.
    Rodhouse JC, Haugh CA, Roberts D, Gilbert RJ. Red kidney bean poisoning in the UK: an analysis of 50 suspected incidents between 1976 and 1989. Epidemiol Infect. 1990;105(3):485–491.CrossRefPubMedGoogle Scholar
  11. 11.
    Banwell JG, Boldt DH, Meyers J, Weber FL Jr. Phytohemagglutinin derived from red kidney bean (Phaseolus vulgaris): a cause for intestinal malabsorption associated with bacterial overgrowth in the rat. Gastroenterology. 1983;84(3):506–515.PubMedGoogle Scholar
  12. 12.
    Banwell JG, Abramowsky CR, Weber F, Howard R, Boldt DH. Phytohemagglutinin-induced diarrheal disease. Dig Dis Sci. 1984;29(10):921–929.CrossRefPubMedGoogle Scholar
  13. 13.
    Hintz HF, Hogue DE, Krook L. Toxicity of red kidney beans (Phaseolus vulgaris) in the rat. J Nutr. 1967;93(1):77–86.PubMedGoogle Scholar
  14. 14.
    Banwell JG, Howard R, Kabir I, Costerton JW. Bacterial overgrowth by indigenous microflora in the phytohemagglutinin-fed rat. Can J Microbiol. 1988;34(8):1009–1013.CrossRefPubMedGoogle Scholar
  15. 15.
    Pusztai A, Grant G, Spencer RJ, et al. Kidney bean lectin-induced Escherichia coli overgrowth in the small intestine is blocked by GNA, a mannose-specific lectin. J Appl Bacteriol. 1993;75(4):360–368.PubMedGoogle Scholar
  16. 16.
    Dobbins JW, Laurenson JP, Gorelick FS, Banwell JG. Phytohemagglutinin from red kidney bean (Phaseolus vulgaris) inhibits sodium and chloride absorption in the rabbit ileum. Gastroenterology. 1986;90(6):1907–1913.PubMedGoogle Scholar
  17. 17.
    Sun Z, Wang X, Andersson R. Role of intestinal permeability in monitoring mucosal barrier function. History, methodology, and significance of pathophysiology. Dig Surg. 1998;15(5):386–397.CrossRefPubMedGoogle Scholar
  18. 18.
    De Lisle RC. Altered transit and bacterial overgrowth in the cystic fibrosis mouse small intestine. Am J Physiol Gastrointest Liver Physiol. 2007;293(1):G104–G111.CrossRefPubMedGoogle Scholar
  19. 19.
    Dokladny K, Moseley PL, Ma TY. Physiologically relevant increase in temperature causes an increase in intestinal epithelial tight junction permeability. Am J Physiol Gastrointest Liver Physiol. 2006;290(2):G204–G212.CrossRefPubMedGoogle Scholar
  20. 20.
    Hart CA, Batt RM, Saunders JR, Getty B. Lectin-induced damage to the enterocyte brush border. An electron-microscopic study in rabbits. Scand J Gastroenterol. 1988;23(10):1153–1159.CrossRefPubMedGoogle Scholar
  21. 21.
    Hendriks HG, Kik MJ, Koninkx JF, van den Ingh TS, Mouwen JM. Binding of kidney bean (Phaseolus vulgaris) isolectins to differentiated human colon carcinoma Caco-2 cells and their effect on cellular metabolism. Gut. 1991;32(2):196–201.CrossRefPubMedGoogle Scholar
  22. 22.
    Rozee KR, Cooper D, Lam K, Costerton JW. Microbial flora of the mouse ileum mucous layer and epithelial surface. Appl Environ Microbiol. 1982;43(6):1451–1463.PubMedGoogle Scholar
  23. 23.
    Kunzelmann K, Sun J, Schreiber R, Konig J. Effects of dietary lectins on ion transport in epithelia. Br J Pharmacol. 2004;142(8):1219–1226.CrossRefPubMedGoogle Scholar
  24. 24.
    Rossi MA, Mancini Filho J, Lajolo FM. Jejunal ultrastructural changes induced by kidney bean (Phaseolus vulgaris) lectins in rats. Br J Exp Pathol. 1984;65(1):117–123.PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media, LLC 2010

Authors and Affiliations

  • Balamurugan Ramadass
    • 1
    • 2
  • Karol Dokladny
    • 2
  • Pope L. Moseley
    • 2
  • Yatin R. Patel
    • 1
    • 2
  • Henry C. Lin
    • 1
    • 2
    Email author
  1. 1.Section of GastroenterologyNew Mexico VA Health Care SystemAlbuquerqueUSA
  2. 2.Department of MedicineUniversity of New MexicoAlbuquerqueUSA

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