Skip to main content

Thank you for visiting 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.

Carbohydrates, glycemic index and diabetes mellitus

Evidence of impaired carbohydrate assimilation in euthyroid patients with Hashimoto’s thyroiditis



Hashimoto’s thyroiditis (HT) represents a wide-spread autoimmune disease. In euthyroid patients with HT, an impaired assimilation of common carbohydrates has been observed. Our objectives were to compare the frequency of (1) fructose (FM), lactose (LM) and sorbitol malassimilation (SM), (2) gastrointestinal symptoms (GS) following carbohydrate ingestion and (3) recurrent GS relevant to the participants’ daily lives.


We conducted a prospective case–control study of 45 ambulatory patients with HT and 38 healthy volunteers, matched with regard to age, gender and area of origin. Hydrogen breath tests with fructose, lactose, sorbitol and glucose were performed, the lactose testing additionally comprising measurements of capillary blood glucose (cBG). GS during the tests and recurrent GS concerning the participants’ daily lives were assessed. A food-frequency questionnaire was administered.


FM was diagnosed in 48.9% of patients compared with 26.3% of the control group (P=0.035). In all, 42.2% of patients with HT and 21.1% of healthy controls showed LM (P=0.04). FM and/or LM was present in 73.3% of the patients and in 42.1% of healthy controls (P=0.004). GS after the ingestion of fructose (P=0.003) or lactose (P=0.025) and recurrent GS were significantly more prevalent in the case group. The consumption of free fructose, lactose or sorbitol did not differ.


Carbohydrate malassimilation and gastrointestinal complaints are frequent in euthyroid patients with HT, leading to novel clinical and pathophysiological considerations and concepts.

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

Access options

Buy article

Get time limited or full article access on ReadCube.


All prices are NET prices.

Figure 1
Figure 2
Figure 3


  1. Latrofa F, Pinchera A . Autoimmune hypothyroidism. In: Weetman AP (ed.) Contemporary Endocrinology: Autoimmune Diseases in Endocrinology. Humana Press: Totowa, NJ, 2008, pp 151–152.

    Google Scholar 

  2. Ebert EC . The thyroid and the gut. J Clin Gastroenterol 2010; 44: 402–406.

    CAS  PubMed  Google Scholar 

  3. Iwen KA, Schroder E, Brant G . Thyroid hormones and the metabolic syndrome. Eur Thyroid J 2013; 2: 83–92.

    Article  Google Scholar 

  4. Matosin-Matekalo M, Mesonero JE, Laroche TJ, Lacasa M, Brot-Laroche E . Glucose and thyroid hormone co-regulate the expression of the intestinal fructose transporter GLUT5. Biochem J 1999; 339: 233–239.

    Article  CAS  Google Scholar 

  5. Mochizuki K, Sakaguchi N, Takabe S, Goda T . De-phosphorylation of TRalpha-1 by p44/42 MAPK inhibition enhances T(3)-mediated GLUT5 gene expression in the intestinal cell line Caco-2 cells. Biochem Biophys Res Commun 2007; 359: 979–984.

    Article  CAS  Google Scholar 

  6. Monteiro IM, Jiang L, Ferraris RP . Dietary modulation of intestinal fructose transport and GLUT5 mRNA expression in hypothyroid rat pups. J Pediatr Gastroenterol Nutr 1999; 29: 563–570.

    Article  CAS  Google Scholar 

  7. Lauritano EC, Bilotta AL, Gabrielli M et al. Association between hypothyroidism and small intestinal bacterial overgrowth. J Clin Endocrinol Metab 2007; 92: 4180–4184.

    Article  CAS  Google Scholar 

  8. Bures J, Cyrany J, Kohoutova D et al. Small intestinal bacterial overgrowth syndrome. World J Gastroenterol 2010; 16: 2978–2990.

    Article  CAS  Google Scholar 

  9. Born P . Carbohydrate malabsorption in patients with non-specific abdominal complaints. World J Gastroenterol 2007; 13: 5687–5691.

    Article  CAS  Google Scholar 

  10. Lomer MC, Parkes GC, Sanderson JD . Lactose intolerance in clinical practice—myths and realities. Aliment Pharmacol Ther 2008; 27: 93–103.

    Article  CAS  Google Scholar 

  11. Gibson PR, Newnham E, Barrett JS, Shepherd SJ, Muir JG . Fructose malabsorption and the bigger picture. Aliment Pharmacol Ther 2007; 25: 349–363.

    Article  CAS  Google Scholar 

  12. Cellini M, Santaguida MG, Gatto I et al. Systematic appraisal of lactose intolerance as cause of increased need for oral thyroxine. J Clin Endocrinol Metab 2014; 99: E1454–E1458.

    Article  CAS  Google Scholar 

  13. Ledochowski M, Widner B, Sperner-Unterweger B, Propst T, Vogel W, Fuchs D . Carbohydrate malabsorption syndromes and early signs of mental depression in females. Dig Dis Sci 2000; 45: 1255–1259.

    Article  CAS  Google Scholar 

  14. Ledochowski M, Uberall F, Propst T, Fuchs D . Fructose malabsorption is associated with lower plasma folic acid concentrations in middle-aged subjects. Clin Chem 1999; 45: 2013–2014.

    CAS  PubMed  Google Scholar 

  15. Ledochowski M, Widner B, Murr C, Fuchs D . Decreased serum zinc in fructose malabsorbers. Clini Chem 2001; 47: 745–747.

    CAS  Google Scholar 

  16. Ledochowski M, Widner B, Propst-Braunsteiner T, Vogel W, Sperner-Unterweger B, Fuchs D . Fructose malabsorption is associated with decreased plasma tryptophan. Adv Exp Med Biol 1999; 467: 73–78.

    Article  CAS  Google Scholar 

  17. Gasbarrini A, Corazza GR, Gasbarrini G et al. Methodology and indications of H2-breath testing in gastrointestinal diseases: the Rome Consensus Conference. Aliment Pharmacol Ther 2009; 29 (Suppl 1), S1–S49.

    Google Scholar 

  18. Lustig RH, Schmidt LA, Brindis CD . Public health: the toxic truth about sugar. Nature 2012; 482: 27–29.

    Article  CAS  Google Scholar 

  19. Vos MB, Kimmons JE, Gillespie C, Welsh J, Blanck HM . Dietary fructose consumption among US children and adults: The Third National Health and Nutrition Examination Survey. Medscape J Med 2008; 10: 160.

    PubMed  PubMed Central  Google Scholar 

  20. Rumessen JJ . Fructose and related food carbohydrates. Sources, intake, absorption, and clinical implications. Scand J Gastroenterol 1992; 27: 819–828.

    Article  CAS  Google Scholar 

  21. Tappy L, Le KA . Metabolic effects of fructose and the worldwide increase in obesity. Physiol Rev 2010; 90: 23–46.

    Article  CAS  Google Scholar 

  22. Stathatos N, Daniels GH . Autoimmune thyroid disease. Curr Opin Rheumatol 2012; 24: 70–75.

    Article  CAS  Google Scholar 

  23. McLeod DS, Cooper DS . The incidence and prevalence of thyroid autoimmunity. Endocrine 2012; 42: 252–265.

    Article  CAS  Google Scholar 

  24. Rizzo M, Rossi RT, Bonaffini O et al. Increased annual frequency of Hashimoto's thyroiditis between years 1988 and 2007 at a cytological unit of Sicily. Ann Endocrinol 2010; 71: 525–534.

    Article  CAS  Google Scholar 

  25. Fink H, Hintze G . Autoimmune thyroiditis (Hashimoto's thyroiditis): current diagnostics and therapy. Med Klin (Munich) 2010; 105: 485–493.

    Article  CAS  Google Scholar 

  26. Braden B . Methods and functions: breath tests. Best Pract Res Clin Gastroenterol 2009; 23: 337–352.

    Article  CAS  Google Scholar 

  27. Brunn J, Block U, Ruf G, Kunze WP . Volumetrie der Schilddrüsenlappen mittels real-time-Sonographie. Dtsch Med Wochenschr 1981; 106: 1338–1340.

    Article  CAS  Google Scholar 

  28. Gutekunst R, Becker A, Hehrmann R, Olbricht T, Pfannenstiel P . Ultraschalldiagnostik der Schilddrüse. Dtsch Med Wochenschr 1988; 113: 1109–1112.

    Article  CAS  Google Scholar 

  29. Wetzel K, H2-Atemtests für die medizinische Forschung und klinische Diagnostik. Fischer Analysen Instrumente GmbH. Available at (accessed 17 October 2014).

  30. Neomed-Medizintechnik. HydroCheck. Available at (accessed 17 October 2014).

  31. Willett W, Nurses' Health Study II 2007. Available at (accessed 17 October 2014).

  32. Asik M, Gunes F, Binnetoglu E et al. Decrease in TSH levels after lactose restriction in Hashimoto's thyroiditis patients with lactose intolerance. Endocrine 2014; 46: 279–284.

    Article  CAS  Google Scholar 

  33. Eisenmann A, Amann A, Said M, Datta B, Ledochowski M . Implementation and interpretation of hydrogen breath tests. J Breath Res 2008; 2: 046002.

    Article  Google Scholar 

  34. Garcia-Herrera J, Marca MC, Brot-Laroche E et al. Protein kinases, TNF-{alpha}, and proteasome contribute in the inhibition of fructose intestinal transport by sepsis in vivo. Am J Physiol Gastrointest Liver Physiol 2008; 294: G155–G164.

    Article  CAS  Google Scholar 

  35. Rho MH, Kim DW, Hong HP et al. Diagnostic value of antithyroid peroxidase antibody for incidental autoimmune thyroiditis based on histopathologic results. Endocrine 2012; 42: 647–652.

    Article  CAS  Google Scholar 

  36. Itan Y, Jones BL, Ingram CJ, Swallow DM, Thomas MG . A worldwide correlation of lactase persistence phenotype and genotypes. BMC Evol Biol 2010; 10: 36.

    Article  Google Scholar 

  37. Terjung B, Lammert F . Lactose intolerance: new aspects of an old problem. Dtsch Med Wochenschr 2007; 132: 271–275.

    Article  CAS  Google Scholar 

  38. Disse SC, Buelow A, Boedeker RH et al. Reduced prevalence of obesity in children with primary fructose malabsorption: a multicentre, retrospective cohort study. Pediatr Obes 2013; 8: 255–258.

    Article  CAS  Google Scholar 

  39. Albuquerque D, Nobrega C, Manco L . The lactase persistence -13910C>T polymorphism shows indication of association with abdominal obesity among Portuguese children. Acta Paediatr 2013; 102: e153–e157.

    Article  CAS  Google Scholar 

  40. Ledochowski M, Murr C, Lass-Florl C, Fuchs D . Increased serum amylase and lipase in fructose malabsorbers. Clin Chim Acta 2001; 311: 119–123.

    Article  CAS  Google Scholar 

  41. Sasso FC, Carbonara O, Torella R et al. Ultrastructural changes in enterocytes in subjects with Hashimoto's thyroiditis. Gut 2004; 53: 1878–1880.

    Article  CAS  Google Scholar 

  42. Prummel MF, Strieder T, Wiersinga WM . The environment and autoimmune thyroid diseases. Eur J Endocrinol 2004; 150: 605–618.

    Article  CAS  Google Scholar 

  43. Mishkin D, Sablauskas L, Yalovsky M, Mishkin S . Fructose and sorbitol malabsorption in ambulatory patients with functional dyspepsia: comparison with lactose maldigestion/malabsorption. Dig Dis Sci 1997; 42: 2591–2598.

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations


Corresponding author

Correspondence to S Heckl.

Ethics declarations

Competing interests

The authors declare no conflict of interest.

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Heckl, S., Reiners, C., Buck, A. et al. Evidence of impaired carbohydrate assimilation in euthyroid patients with Hashimoto’s thyroiditis. Eur J Clin Nutr 70, 222–228 (2016).

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI:


Quick links