Influence of chronic diseases on the olfactory function in children

European Journal of Pediatrics volume 178, pages1185–1193(2019)Cite this article

Abstract

The association between smell impairment and chronic diseases has been reported in some studies in adults. Such information is not available for chronic diseases in children. The aim of this study was to examine olfactory function of children with chronic diseases such as diabetes mellitus type 1, hypothyroidism, and bronchial asthma in combination with allergic rhinitis in comparison to healthy controls. The data were obtained from n = 205 participants (104 boys, 101 girls) between the age of 6 and 17 years. Seventy-eight of the participants were healthy controls, n = 43 had diabetes mellitus type 1, n = 50 suffer from allergic rhinitis or bronchial asthma, and 34 presented a reduced function of their thyroid in medical history. All participants underwent olfactory testing including olfactory threshold using “Sniffin’ Sticks” and odor identification using the “U-Sniff” test. In addition, a depression inventory and cognitive testing using the Ravens Progressive Matrices was performed. No significant difference in olfactory function was observed for any of the chronic diseases in children in comparison to healthy controls. Further analysis showed a trend in significance for a subpopulation of children with bronchial asthma and comorbidities performed worse on the olfactory threshold test compared to patients with bronchial asthma without comorbidities. Pediatric patients suffering from chronic diseases scored higher on the depression inventory compared to healthy controls.

Conclusion: In conclusion, this study demonstrates that the influence of chronic diseases (bronchial asthma, diabetes mellitus type 1 and hypothyroidism) on olfactory function in childhood, if any, seems to be insignificant. This is partly in contrast to adult patients. Further research should be conducted in a subgroup of patients with bronchial asthma, allergic rhinitis, and atopic dermatitis or other comorbidities to better understand the association of allergic diathesis and olfactory function and the putative pathogenesis of olfactory dysfunction.

What is known:
• The association between smell impairment and chronic diseases has been reported in some studies in adults.
• Such information is not available for chronic diseases in children.
What is new:
• The influence of chronic diseases (bronchial asthma, diabetes mellitus type 1, and hypothyroidism) on olfactory function in childhood, if any, seems to be insignificant.
• In patients with bronchial asthma and allergic rhinitis, only a subgroup of patients with additional comorbidity (atopic dermatitis) showed a tendency to a reduced sense of smell.

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

Access options

Buy single article

Instant access to the full article PDF.

US$ 39.95

Tax calculation will be finalised during checkout.

Abbreviations

CPM:

Colored progressive matrices

F:

Degrees of freedom

fT3:

Free triiodothyronine

fT4:

Tetraiodothyronine

HbA1c:

Glycohemoglobin A1c

MANOVA:

Multivariate variance analysis

n:

Amount

p:

Significance level

r:

Correlation coefficient

SD:

Standard deviation

SPM:

Standard progressive matrices

SPSS:

Statistical Package for the Social Sciences

TSH:

Thyroid-stimulating hormone

U-Sniff:

universal Sniffin’ Sticks Test for children

References

  1. 1.

    Aj A, Ae M, Me F, Jm C (1995) Allergic rhinitis and olfactory loss. Ann Allergy Asthma Immunol 75:311–316

    Google Scholar 

  2. 2.

    Altundag A, Cayonu M, Kayabasoglu G, Salihoglu M, Tekeli H, Saglam O, Hummel T (2015) Modified olfactory training in patients with postinfectious olfactory loss. Laryngoscope 125:1763–1766. https://doi.org/10.1002/lary.25245

    Article  PubMed  Google Scholar 

  3. 3.

    Altundag A, Ay SA, Hira S, Salıhoglu M, Baskoy K, Denız F, Tekelı H, Kurt O, Yonem A, Hummel T (2017) Olfactory and gustatory functions in patients with non-complicated type 1 diabetes mellitus. Eur Arch Otorhinolaryngol 274:2621–2627. https://doi.org/10.1007/s00405-017-4497-8

    Article  PubMed  Google Scholar 

  4. 4.

    Armstrong JE, Laing DG, Wilkes FJ, Kainer G (2010) Smell and taste function in children with chronic kidney disease. Pediatr Nephrol Berl Ger 25:1497–1504. https://doi.org/10.1007/s00467-010-1529-7

    Article  Google Scholar 

  5. 5.

    Beard MD, Mackay-Sim A (1987) Loss of sense of smell in adult, hypothyroid mice. Dev Brain Res 36:181–189. https://doi.org/10.1016/0165-3806(87)90022-8

    Article  CAS  Google Scholar 

  6. 6.

    Brosvic GM, Risser JM, Mackay-Sim A, Doty RL (1996) Odor detection performance in hypothyroid and euthyroid rats. Physiol Behav 59:117–121. https://doi.org/10.1016/0031-9384(95)00145-X

    Article  CAS  PubMed  Google Scholar 

  7. 7.

    Cowart B, Flynnrodden K, Mcgeady S, Lowry L (1993) Hyposmia in allergic rhinitis. J Allergy Clin Immunol 91:747–751. https://doi.org/10.1016/0091-6749(93)90194-K

    Article  CAS  Google Scholar 

  8. 8.

    Croy I, Symmank A, Schellong J, Hummel C, Gerber J, Joraschky P, Hummel T (2014) Olfaction as a marker for depression in humans. J Affect Disord 160:80–86. https://doi.org/10.1016/j.jad.2013.12.026

    Article  Google Scholar 

  9. 9.

    Deniz F, Ay SA, Salihoglu M, Kurt O, Baskoy K, Altundag A, Tekeli H, Yonem A, Hummel T (2016) Thyroid hormone replacement therapy improves olfaction and taste sensitivity in primary hypothyroid patients: a prospective randomised clinical trial. Exp Clin Endocrinol Diabetes 124:562–567. https://doi.org/10.1055/s-0042-108446

    Article  CAS  PubMed  Google Scholar 

  10. 10.

    Doty RL, Mishra A (2001) Olfaction and its alteration by nasal obstruction, rhinitis, and rhinosinusitis. Laryngoscope 111:409–423. https://doi.org/10.1097/00005537-200103000-00008

    Article  CAS  PubMed  Google Scholar 

  11. 11.

    Enwere E, Shingo T, Gregg C, Fujikawa H, Ohta S, Weiss S (2004) Aging results in reduced epidermal growth factor receptor signaling, diminished olfactory neurogenesis, and deficits in fine olfactory discrimination. J Neurosci 24:8354–8365. https://doi.org/10.1523/JNEUROSCI.2751-04.2004

    Article  CAS  PubMed  Google Scholar 

  12. 12.

    Fischer M, Zopf Y, Elm C, Pechmann G, Hahn EG, Schwab D, Kornhuber J, Thuerauf NJ (2014) Subjective and objective olfactory abnormalities in Crohn’s disease. Chem Senses 39:529–538. https://doi.org/10.1093/chemse/bju022

    Article  CAS  PubMed  Google Scholar 

  13. 13.

    Floch J-PL, Lièvre GL, Labroue M, Paul M, Peynegre R, Perlemuter L (1993) Smell dysfunction and related factors in diabetic patients. Diabetes Care 16:934–937. https://doi.org/10.2337/diacare.16.6.934

    Article  PubMed  Google Scholar 

  14. 14.

    Gellrich J, Stetzler C, Oleszkiewicz A, Hummel T, Schriever VA (2017) Olfactory threshold and odor discrimination ability in children – evaluation of a modified “Sniffin’ Sticks” test. Sci Rep 7(1928):1928. https://doi.org/10.1038/s41598-017-01465-1

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. 15.

    Gouveri E, Katotomichelakis M, Gouveris H, Danielides V, Maltezos E, Papanas N (2014) Olfactory dysfunction in type 2 diabetes mellitus: an additional manifestation of microvascular disease? Angiology 65:869–876. https://doi.org/10.1177/0003319714520956

    Article  CAS  PubMed  Google Scholar 

  16. 16.

    Guilemany JM, García-Piñero A, Alobid I, Cardelús S, Centellas S, Bartra J, Valero A, Picado C, Mullol J (2009) Persistent allergic rhinitis has a moderate impact on the sense of smell, depending on both nasal congestion and inflammation. Laryngoscope 119:233–238. https://doi.org/10.1002/lary.20075

    Article  CAS  Google Scholar 

  17. 17.

    Guss J, Doghramji L, Reger C, Chiu AG (2009) Olfactory dysfunction in allergic rhinitis. ORL J Oto-Rhino-Laryngol Relat Spec 71:268–272. https://doi.org/10.1159/000242429

    Article  Google Scholar 

  18. 18.

    Härter MC (2000) Psychische Störungen bei körperlichen Erkrankungen. PPmP - Psychother Psychosom Med Psychol 50:274–286. https://doi.org/10.1055/s-2000-8822

    Article  Google Scholar 

  19. 19.

    Hedner M, Larsson M, Arnold N, Zucco GM, Hummel T (2010) Cognitive factors in odor detection, odor discrimination, and odor identification tasks. J Clin Exp Neuropsychol 32:1062–1067. https://doi.org/10.1080/13803391003683070

    Article  Google Scholar 

  20. 20.

    Hummel T, Nordin S (2005) Olfactory disorders and their consequences for quality of life. Acta Otolaryngol (Stockh) 125:116–121. https://doi.org/10.1080/00016480410022787

    Article  Google Scholar 

  21. 21.

    Hummel T, Sekinger B, Wolf SR, Pauli E, Kobal G (1997) ‘Sniffin’ Sticks’: olfactory performance assessed by the combined testing of odour identification, odor discrimination and olfactory threshold. Chem Senses 22:39–52. https://doi.org/10.1093/chemse/22.1.39

    Article  CAS  Google Scholar 

  22. 22.

    Hummel T, Kobal G, Gudziol H, Mackay-Sim A (2007) Normative data for the “Sniffin’ Sticks” including tests of odor identification, odor discrimination, and olfactory thresholds: an upgrade based on a group of more than 3,000 subjects. Eur Arch Otorhinolaryngol 264:237–243. https://doi.org/10.1007/s00405-006-0173-0

    Article  CAS  Google Scholar 

  23. 23.

    Hüttenbrink KB (2008) Riech- und Schmeckstörungen - Bewährtes und Neues zu Diagnostik und Therapie*. Laryngo-Rhino-Otol. 76:506–514. https://doi.org/10.1055/s-2007-997469

    Article  Google Scholar 

  24. 24.

    Izquierdo-Dominguez A, Jauregui I, Del Cuvillo A, Montoro J, Davila I, Sastre J, Bartra J, Ferrer M, Alobid I, Mullol J, Valero AL (2017) Allergy rhinitis: similarities and differences between children and adults. Rhinology. 55:326–331. https://doi.org/10.4193/Rhin17.074

    Article  CAS  PubMed  Google Scholar 

  25. 25.

    Keller F, Grieb J, Ernst M, Spröber N, Fegert JM, Kölch M (2011) Children’s depression rating scale – revised (CDRS-R). Z Für Kinder- Jugendpsychiatrie Psychother 39:179–185. https://doi.org/10.1024/1422-4917/a000090

    Article  Google Scholar 

  26. 26.

    Kobal G, Hummel T, Sekinger B, Barz S, Roscher S, Wolf S (1996) “Sniffin’ Sticks”: screening of olfactory performance. Rhinology 34:222–226

    CAS  Google Scholar 

  27. 27.

    Koseoglu S, Derin S, Huddam B, Sahan M (2017) The effect of non-diabetic chronic renal failure on olfactory function. Eur Ann Otorhinolaryngol Head Neck Dis 134:161–164. https://doi.org/10.1016/j.anorl.2016.04.022

    Article  CAS  PubMed  Google Scholar 

  28. 28.

    Kratzmeier H, Horn R (1988) Standard progressive matrices manual. Auflage. ed. Beltz Test Gesellschaft, Weinheim, p 2

    Google Scholar 

  29. 29.

    Kutlug S, Gunbey E, Sogut A, Celiksoy MH, Kardas S, Yildirim U, Karli R, Murat N, Sancak R (2016) Evaluation of olfactory function in children with allergic rhinitis and nonallergic rhinitis. Int J Pediatr Otorhinolaryngol 86:172–176. https://doi.org/10.1016/j.ijporl.2016.04.038

    Article  PubMed  Google Scholar 

  30. 30.

    Langdon C, Guilemany JM, Valls M, Alobid I, Bartra J, Dávila I, Del Cuvillo A, Ferrer M, Jáuregui I, Montoro J, Sastre J, Valero A, Mullol J (2016) Allergic rhinitis causes loss of smell in children: the OLFAPEDRIAL study. Pediatr Allergy Immunol 27:867–870. https://doi.org/10.1111/pai.12655

    Article  PubMed  Google Scholar 

  31. 31.

    Loo AT, Youngentob SL, Kent PF, Schwob JE (1996) The aging olfactory epithelium: neurogenesis, response to damage, and odorant-induced activity. Int J Dev Neurosci 14:881–900. https://doi.org/10.1016/S0736-5748(96)00046-9

    Article  CAS  PubMed  Google Scholar 

  32. 32.

    Mackay-Sim A, Beard MD (1987) Hypothyroidism disrupts neural development in the olfactory epithelium of adult mice. Dev Brain Res 36:190–198. https://doi.org/10.1016/0165-3806(87)90023-X

    Article  CAS  Google Scholar 

  33. 33.

    Marschner H, Gudziol H, Guntinas-Lichius O (2010) Riechstörungen sind wesentlich häufiger als sie beklagt werden. Laryngo-Rhino-Otol. 89:654–659. https://doi.org/10.1055/s-0030-1262779

    Article  CAS  Google Scholar 

  34. 34.

    McConnell RJ, Menendez CE, Smith FR, Henkin RI, Rivlin RS (1975) Defects of taste and smell in patients with hypothyroidism. Am J Med 59:354–364. https://doi.org/10.1016/0002-9343(75)90394-0

    Article  CAS  PubMed  Google Scholar 

  35. 35.

    Naka A, Riedl M, Luger A, Hummel T, Mueller CA (2010) Clinical significance of smell and taste disorders in patients with diabetes mellitus. Eur Arch Otorhinolaryngol 267:547–550. https://doi.org/10.1007/s00405-009-1123-4

    Article  PubMed  Google Scholar 

  36. 36.

    Oral E, Aydin MD, Aydin N, Ozcan H, Hacimuftuoglu A, Sipal S, Demirci E (2013) How olfaction disorders can cause depression? The role of habenular degeneration. Neuroscience 240:63–69. https://doi.org/10.1016/j.neuroscience.2013.02.026

    Article  CAS  PubMed  Google Scholar 

  37. 37.

    Pind J, Gunnarsdóttir EK, Jóhannesson HS (2003) Raven’s standard progressive matrices: new school age norms and a study of the test’s validity. Personal Individ Differ 34:375–386. https://doi.org/10.1016/S0191-8869(02)00058-2

    Article  Google Scholar 

  38. 38.

    Raven J (2000) The Raven’s progressive matrices: change and stability over culture and time. Cognit Psychol 41:1–48. https://doi.org/10.1006/cogp.1999.0735

    Article  CAS  PubMed  Google Scholar 

  39. 39.

    Raven JC, Raven J, Court JH (2001) Coloured progressive matrices Stephan Bulheller, Hartmut Häcke

  40. 40.

    Schriever VA, Agosin E, Altundag A, Avni H, Cao Van H, Cornejo C, de Los Santos G, Fishman G, Fragola C, Guarneros M, Gupta N, Hudson R, Kamel R, Knaapila A, Konstantinidis I, Landis BN, Larsson M, Lundström JN, Macchi A, Mariño-Sánchez F, Martinec Nováková L, Mori E, Mullol J, Nord M, Parma V, Philpott C, Propst EJ, Rawan A, Sandell M, Sorokowska A, Sorokowski P, Sparing-Paschke L-M, Stetzler C, Valder C, Vodicka J, Hummel T (2018) Development of an international odor identification test for children: the universal sniff test. J Pediatr 198:265–272.e3. https://doi.org/10.1016/j.jpeds.2018.03.011

    Article  Google Scholar 

  41. 41.

    Schwob JE (2002) Neural regeneration and the peripheral olfactory system. Anat Rec 269:33–49. https://doi.org/10.1002/ar.10047

    Article  PubMed  Google Scholar 

  42. 42.

    Simola M, Malmberg H (1998) Sense of smell in allergic and nonallergic rhinitis. Allergy 53:190–194

    Article  CAS  Google Scholar 

  43. 43.

    Steinbach S, Reindl W, Dempfle A, Schuster A, Wolf P, Hundt W, Huber W (2013) Smell and taste in inflammatory bowel disease. PLoS One 8:e73454. https://doi.org/10.1371/journal.pone.0073454

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  44. 44.

    Stevenson RJ (2010) An initial evaluation of the functions of human olfaction. Chem Senses 35:3–20. https://doi.org/10.1093/chemse/bjp083

    Article  Google Scholar 

  45. 45.

    Stuck BA, Hummel T (2015) Olfaction in allergic rhinitis: a systematic review. J Allergy Clin Immunol 136:1460–1470. https://doi.org/10.1016/j.jaci.2015.08.003

    Article  PubMed  Google Scholar 

  46. 46.

    Weinstock RS, Wright HN, Smith DU (1993) Olfactory dysfunction in diabetes mellitus. Physiol Behav 53:17–21. https://doi.org/10.1016/0031-9384(93)90005-Z

    Article  CAS  PubMed  Google Scholar 

  47. 47.

    Whitcroft KL, Cuevas M, Haehner A, Hummel T (2017) Patterns of olfactory impairment reflect underlying disease etiology. Laryngoscope 127:291–295. https://doi.org/10.1002/lary.26229

    Article  Google Scholar 

Download references

Funding

Funding was provided to VAS from the Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden (MedDrive) and the Else Kröner-Fresenius-Stiftung.

MLD received financial support from the Graduiertenakademie from the Technische Universität Dresden.

Author information

Affiliations

  1. Abteilung Neuropädiatrie, Medizinische Fakultät Carl Gustav Carus, Technische Universität Dresden, Fetscherstrasse 74, 01307, Dresden, Germany

    Janine Gellrich, Marie-Luise Dabow, Maja von der Hagen & Valentin A. Schriever

  2. Klinik und Poliklinik für Kinder- und Jugendmedizin, Medizinische Fakultät Carl Gustav Carus, Technische Universität, Dresden, Dresden, Germany

    Janine Gellrich, Christian Vogelberg, Felix Reschke & Andrea Näke

Authors
  1. Janine Gellrich
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Marie-Luise Dabow
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Christian Vogelberg
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Felix Reschke
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andrea Näke
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Maja von der Hagen
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Valentin A. Schriever
    View author publications

    You can also search for this author in PubMed Google Scholar

Contributions

Janine Gellrich: author, data management, statistical analysis of the data.Marie-Luise Dabow: Recruitment of volunteers, data collection, data management, critical review. Christian Vogelberg: critical review and advice in relation to allergic rhinitis and asthma.Felix Reschke: critical review and advice in relation to endocrinological issues.Andrea Näke: critical review and advice in relation to diabetes.Maja von der Hagen: critical review and planning of the study.Valentin A. Schriever: planning of the study, statistical analysis, critical review.

Corresponding author

Correspondence to Janine Gellrich.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical consent

The study was conducted in accordance with the Declaration of Helsinki on Biomedical Studies Involving Human Subjects. The consent of all individuals involved in the study has been obtained after information. This article does not include studies with animals conducted by any of the authors.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Communicated by Peter de Winter

Rights and permissions

Reprints and Permissions

About this article

Verify currency and authenticity via CrossMark

Cite this article

Gellrich, J., Dabow, ML., Vogelberg, C. et al. Influence of chronic diseases on the olfactory function in children. Eur J Pediatr 178, 1185–1193 (2019). https://doi.org/10.1007/s00431-019-03380-1

Download citation

Keywords

  • Olfactory threshold
  • Odor identification
  • “Sniffin’ sticks”
  • Chronic diseases children
  • Bronchial asthma
  • Allergic rhinosinusitis
  • Hypothyroidism
  • Diabetes mellitus type 1
  • Children