Skip to main content

A systematic review on olfaction in child and adolescent psychiatric disorders

Journal of Neural Transmission volume 120, pages 121–130 (2013)Cite this article

Abstract

There is substantial evidence that olfactory function may serve as biomarker in adult neuropsychiatric disorders, e.g. overall diminished olfaction in Parkinson’s disease as parameter for early pre-motor and differential diagnosis. Here, we present data from a systematic literature review in olfactory function in child and adolescent psychiatric disorders and report two unpublished data sets of autism and obsessive–compulsive disorder. The overall number of olfaction studies is low—even after taking into account adult samples. In addition, heterogeneity of findings is high due to methodological limitations such as the use of different olfactory tests and odours targeting the olfactory and/or the trigeminal system and neglecting possible confounders, e.g., intelligence or oto-rhino-laryngological affections. Despite these limitations, there is some indication for specific alterations of olfactory function especially in disorders with dopaminergic pathology (e.g. attention deficit/hyperactivity disorder, autism, schizophrenia, 22q11 deletion syndrome). Dopamine is a relevant modulator of early processes in the olfactory bulb. Our systematic review provides the basis for future confirmatory studies investigating olfaction as putative biomarker in child and adolescent psychiatric disorders. We further propose studies of thorough and elaborate methodological standards in combination with imaging techniques and the investigation of the influence of genetic variation on olfactory function.

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

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

References

  • Albrecht J, Wiesmann M (2006) The human olfactory system. Anatomy and physiology. Nervenarzt 77(8):931–939

    PubMed  Article  CAS  Google Scholar 

  • Aschenbrenner K, Scholze N, Joraschky P, Hummel T (2008) Gustatory and olfactory sensitivity in patients with anorexia and bulimia in the course of treatment. J Psychiatr Res 43(2):129–137

    PubMed  Article  Google Scholar 

  • Atanasova B, Graux J, El Hage W, Hommet C, Camus V, Belzung C (2008) Olfaction: a potential cognitive marker of psychiatric disorders. Neurosci Biobehav Rev 32(7):1315–1325

    PubMed  Article  Google Scholar 

  • Barnett R, Maruff P, Purcell R, Wainwright K, Kyrios M, Brewer W, Pantelis C (1999) Impairment of olfactory identification in obsessive-compulsive disorder. Psychol Med 29(5):1227–1233

    PubMed  Article  CAS  Google Scholar 

  • Bennetto L, Kuschner ES, Hyman SL (2007) Olfaction and taste processing in autism. Biol Psychiatry 62(9):1015–1021

    PubMed  Article  Google Scholar 

  • Borta A, Hoglinger GU (2007) Dopamine and adult neurogenesis. J Neurochem 100(3):587–595

    PubMed  Article  CAS  Google Scholar 

  • Brand G (2006) Olfactory/trigeminal interactions in nasal chemoreception. Neurosci Biobehav Rev 30(7):908–917

    PubMed  Article  Google Scholar 

  • Brewer WJ, Wood SJ, McGorry PD, Francey SM, Phillips LJ, Yung AR, Anderson V, Copolov DL, Singh B, Velakoulis D, Pantelis C (2003) Impairment of olfactory identification ability in individuals at ultra-high risk for psychosis who later develop schizophrenia. Am J Psychiatry 160(10):1790–1794

    PubMed  Article  Google Scholar 

  • Brewer WJ, Castle D, Pantelis C (2006) Olfaction and the Brain. University Press, Cambridge

    Book  Google Scholar 

  • Brewer WJ, Pantelis C (2010) Olfactory sensitivity: functioning in schizophrenia and implications for understanding the nature and progression of psychosis. Vitam Horm 83:305–329

    PubMed  Article  CAS  Google Scholar 

  • Cabeza R, Nyberg L (2000) Neural bases of learning and memory: functional neuroimaging evidence. Curr Opin Neurol 13(4):415–421

    PubMed  Article  CAS  Google Scholar 

  • Cave JW, Baker H (2009) Dopamine systems in the forebrain. Adv Exp Med Biol 651:15–35

    PubMed  Article  CAS  Google Scholar 

  • Clepce M, Reich K, Gossler A, Kornhuber J, Thuerauf N (2012) Olfactory abnormalities in anxiety disorders. Neurosci Lett 511(1):43–46

    PubMed  Article  CAS  Google Scholar 

  • Corcoran C, Whitaker A, Coleman E, Fried J, Feldman J, Goudsmit N, Malaspina D (2005) Olfactory deficits, cognition and negative symptoms in early onset psychosis. Schizophr Res 80(2–3):283–293

    PubMed  Article  Google Scholar 

  • Doty RL (2007) Olfaction in Parkinson’s disease. Parkinsonism Relat Disord 13(Suppl 3):S225–S228

    PubMed  Article  Google Scholar 

  • Dudova I, Vodicka J, Havlovicova M, Sedlacek Z, Urbanek T, Hrdlicka M (2011) Odor detection threshold, but not odor identification, is impaired in children with autism. Eur Child Adolesc Psychiatry 20(7):333–340

    PubMed  Article  Google Scholar 

  • Dulay MF, Gesteland RC, Shear PK, Ritchey PN, Frank RA (2008) Assessment of the influence of cognition and cognitive processing speed on three tests of olfaction. J Clin Exp Neuropsychol 30(3):327–337

    PubMed  Article  Google Scholar 

  • Fedoroff IC, Stoner SA, Andersen AE, Doty RL, Rolls BJ (1995) Olfactory dysfunction in anorexia and bulimia nervosa. Int J Eat Disord 18(1):71–77

    PubMed  Article  CAS  Google Scholar 

  • Fenger MM, Gade A, Adams KH, Hansen ES, Bolwig TG, Knudsen GM (2005) Cognitive deficits in obsessive–compulsive disorder on tests of frontal lobe functions. Nord J Psychiatry 59(1):39–44

    PubMed  Article  Google Scholar 

  • Gansler DA, Fucetola R, Krengel M, Stetson S, Zimering R, Makary C (1998) Are there cognitive subtypes in adult attention deficit/hyperactivity disorder? J Nerv Ment Dis 186(12):776–781

    PubMed  Article  CAS  Google Scholar 

  • Gheusi G, Lledo PM (2007) Control of early events in olfactory processing by adult neurogenesis. Chem Senses 32(4):397–409

    PubMed  Article  Google Scholar 

  • Goldberg ED, Goldberg RJ, Vannoppen B (1991) Sense of smell and obsessional behavior. Am J Psychiatry 148(12):1757

    PubMed  CAS  Google Scholar 

  • Good KP, Whitehorn D, Rui Q, Milliken H, Kopala LC (2006) Olfactory identification deficits in first-episode psychosis may predict patients at risk for persistent negative and disorganized or cognitive symptoms. Am J Psychiatry 163(5):932–933

    PubMed  Article  Google Scholar 

  • Gross-Isseroff R, Luca-Haimovici K, Sasson Y, Kindler S, Kotler M, Zohar J (1994) Olfactory sensitivity in major depressive disorder and obsessive compulsive disorder. Biol Psychiatry 35(10):798–802

    PubMed  Article  CAS  Google Scholar 

  • Group BDW (2001) Biomarkers and surrogate endpoints: preferred definitions and conceptual framework. Clin Pharmacol Ther 69(3):89–95

    Article  Google Scholar 

  • 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(10):1062–1067

    PubMed  Article  Google Scholar 

  • Hermesh H, Zohar J, Weizman A, Voet H, Gross-Isseroff R (1999) Orbitofrontal cortex dysfunction in obsessive-compulsive disorder? II. Olfactory quality discrimination in obsessive–compulsive disorder. Eur Neuropsychopharmacol 9(5):415–420

    PubMed  Article  CAS  Google Scholar 

  • Huisman E, Uylings HB, Hoogland PV (2004) A 100% increase of dopaminergic cells in the olfactory bulb may explain hyposmia in Parkinson’s disease. Mov Disord 19(6):687–692

    PubMed  Article  Google Scholar 

  • Kageyama R, Imayoshi I, Sakamoto M (2012) The role of neurogenesis in olfaction-dependent behaviors. Behav Brain Res 227(2):459–463

    PubMed  Article  Google Scholar 

  • Kamath V, Turetsky BI, Calkins ME, Kohler CG, Conroy CG, Borgmann-Winter K, Gatto DE, Gur RE, Moberg PJ (2011) Olfactory processing in schizophrenia, non-ill first-degree family members, and young people at-risk for psychosis. World J Biol Psychiatry. doi:10.3109/15622975.2011.615862

  • Kamath V, Moberg PJ, Gur RE, Doty RL, Turetsky BI (2012) Effects of the val(158)met catechol-O-methyltransferase gene polymorphism on olfactory processing in schizophrenia. Behav Neurosci 126(1):209–215

    PubMed  Article  CAS  Google Scholar 

  • Kareken DA, Mosnik DM, Doty RL, Dzemidzic M, Hutchins GD (2003) Functional anatomy of human odor sensation, discrimination, and identification in health and aging. Neuropsychology 17(3):482–495

    PubMed  Article  Google Scholar 

  • Karsz FR, Vance A, Anderson VA, Brann PG, Wood SJ, Pantelis C, Brewer WJ (2008) Olfactory impairments in child attention-deficit/hyperactivity disorder. J Clin Psychiatry 69(9):1462–1468

    PubMed  Article  Google Scholar 

  • Kopala LC, Good KP (1996) Olfactory identification ability in patients with panic disorder. J Psychiatry Neurosci 21(5):340–342

    PubMed  CAS  Google Scholar 

  • Kopala LC, Good KP, Honer WG (1994) Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophr Res 12(3):205–211

    PubMed  Article  CAS  Google Scholar 

  • Kopala LC, Good K, Goldner EM, Birmingham CL (1995) Olfactory identification ability in anorexia nervosa. J Psychiatry Neurosci 20(4):283–286

    PubMed  CAS  Google Scholar 

  • Kosaka T, Kosaka K (2011) “Interneurons” in the olfactory bulb revisited. Neurosci Res 69(2):93–99

    PubMed  Article  CAS  Google Scholar 

  • Kranick SM, Duda JE (2008) Olfactory dysfunction in Parkinson’s disease. Neurosignals 16(1):35–40

    PubMed  Article  CAS  Google Scholar 

  • Lombion-Pouthier S, Vandel P, Nezelof S, Haffen E, Millot JL (2006) Odor perception in patients with mood disorders. J Affect Disord 90(2–3):187–191

    PubMed  Article  Google Scholar 

  • May T, Brewer WJ, Rinehart NJ, Enticott PG, Brereton AV, Tonge BJ (2011) Differential olfactory identification in children with autism and Asperger’s disorder: a comparative and longitudinal study. J Autism Dev Disord 41(7):837–847

    PubMed  Article  Google Scholar 

  • Murphy KR, Barkley RA, Bush T (2001) Executive functioning and olfactory identification in young adults with attention deficit-hyperactivity disorder. Neuropsychology 15(2):211–220

    PubMed  Article  CAS  Google Scholar 

  • Rapps N, Giel KE, Sohngen E, Salini A, Enck P, Bischoff SC, Zipfel S (2010) Olfactory deficits in patients with anorexia nervosa. Eur Eat Disord Rev 18(5):385–389

    PubMed  Article  Google Scholar 

  • Roessner V, Bleich S, Banaschewski T, Rothenberger A (2005) Olfactory deficits in anorexia nervosa. Eur Arch Psychiatry Clin Neurosci 255(1):6–9

    PubMed  Article  Google Scholar 

  • Romanos M, Renner TJ, Schecklmann M, Hummel B, Roos M, von Mering C, Pauli P, Reichmann H, Warnke A, Gerlach M (2008) Improved odor sensitivity in attention-deficit/hyperactivity disorder. Biol Psychiatry 64(11):938–940

    PubMed  Article  CAS  Google Scholar 

  • Romanos M, Schecklmann M, Kraus K, Fallgatter AJ, Warnke A, Lesch KP, Gerlach M (2011) Olfactory deficits in deletion syndrome 22q11.2. Schizophr Res 129(2–3):220–221

    PubMed  Article  Google Scholar 

  • Schecklmann M, Schaldecker M, Aucktor S, Brast J, Kirchgassner K, Muhlberger A, Warnke A, Gerlach M, Fallgatter AJ, Romanos M (2011a) Effects of methylphenidate on olfaction and frontal and temporal brain oxygenation in children with ADHD. J Psychiatr Res 45(11):1463–1470

    PubMed  Article  Google Scholar 

  • Schecklmann M, Schenk E, Maisch A, Kreiker S, Jacob C, Warnke A, Gerlach M, Fallgatter AJ, Romanos M (2011b) Altered frontal and temporal brain function during olfactory stimulation in adult attention-deficit/hyperactivity disorder. Neuropsychobiology 63(2):66–76

    PubMed  Article  Google Scholar 

  • Schecklmann M, Pfannstiel C, Fallgatter AJ, Warnke A, Gerlach M, Romanos M (2012) Olfaction in child and adolescent anorexia nervosa. J Neural Transm 119(6):721–728

    PubMed  Article  Google Scholar 

  • Schreder T, Albrecht J, Kleemann AM, Schopf V, Kopietz R, Anzinger A, Demmel M, Linn J, Pollatos O, Wiesmann M (2008) Olfactory performance of patients with anorexia nervosa and healthy subjects in hunger and satiety. Rhinology 46(3):175–183

    PubMed  Google Scholar 

  • Segalas C, Labad J, Alonso P, Real E, Subira M, Bueno B, Jimenez-Murcia S, Menchon JM (2011) Olfactory identification and discrimination in obsessive–compulsive disorder. Depress Anxiety 28(10):932–940

    PubMed  Article  Google Scholar 

  • Sobin C, Kiley-Brabeck K, Dale K, Monk SH, Khuri J, Karayiorgou M (2006) Olfactory disorder in children with 22q11 deletion syndrome. Pediatrics 118(3):e697–e703

    PubMed  Article  Google Scholar 

  • Stockhorst U, Pietrowsky R (2004) Olfactory perception, communication, and the nose-to-brain pathway. Physiol Behav 83(1):3–11

    PubMed  CAS  Google Scholar 

  • Suzuki Y, Critchley HD, Rowe A, Howlin P, Murphy DG (2003) Impaired olfactory identification in Asperger’s syndrome. J Neuropsychiatry Clin Neurosci 15(1):105–107

    PubMed  Article  Google Scholar 

  • Tavassoli T, Baron-Cohen S (2012) Olfactory detection thresholds and adaptation in adults with autism spectrum condition. J Autism Dev Disord 42(6):905–909

    PubMed  Article  CAS  Google Scholar 

  • Turetsky BI, Crutchley P, Walker J, Gur RE, Moberg PJ (2009) Depth of the olfactory sulcus: a marker of early embryonic disruption in schizophrenia? Schizophr Res 115(1):8–11

    PubMed  Article  Google Scholar 

  • Weiland R, Macht M, Ellgring H, Gross-Lesch S, Lesch KP, Pauli P (2011) Olfactory and gustatory sensitivity in adults with attention-deficit/hyperactivity disorder. Atten Defic Hyperact Disord 3(1):53–60

    PubMed  Article  Google Scholar 

  • Whitman MC, Greer CA (2007) Adult-generated neurons exhibit diverse developmental fates. Dev Neurobiol 67(8):1079–1093

    PubMed  Article  CAS  Google Scholar 

  • Winner B, Geyer M, Couillard-Despres S, Aigner R, Bogdahn U, Aigner L, Kuhn G, Winkler J (2006) Striatal deafferentation increases dopaminergic neurogenesis in the adult olfactory bulb. Exp Neurol 197(1):113–121

    PubMed  Article  CAS  Google Scholar 

  • Woodberry KA, Seidman LJ, Giuliano AJ, Verdi MB, Cook WL, McFarlane WR (2010) Neuropsychological profiles in individuals at clinical high risk for psychosis: relationship to psychosis and intelligence. Schizophr Res 123(2–3):188–198

    PubMed  Article  Google Scholar 

  • Zernecke R, Vollmer B, Albrecht J, Kleemann AM, Haegler K, Linn J, Fesl G, Bruckmann H, Wiesmann M (2010) Comparison of two different odorants in an olfactory detection threshold test of the Sniffin’ Sticks. Rhinology 48(3):368–373

    PubMed  CAS  Google Scholar 

Download references

Acknowledgments

This work has been accomplished as part of the medical doctoral thesis of Sebastian Volkmann and the psychological diploma thesis of Bettina Hummel. This work was supported by an editorial grant of the Münchner Medizinische Wochenzeitschrift. We also want to thank numerous doctoral candidates and psychological diplomates without their intensive efforts this work would not have been possible: Bettina Hummel, Miriam Roos, Christoph Pfannstiel, Maria Reidelbach, Katharina Kirchgäßner, Susanne Aucktor, Matthias Schaldecker, Eva Schenk, Julia Brast, Katharina Kraus, Laura Albantakis, Lennart Reefschläger and Benjamin Lyttwin. We thank all children and adults who spent their time for participation in our studies.

Author information

Affiliations

  1. Department of Psychiatry and Psychotherapy, University of Regensburg, Universitätsstraße 84, 93053, Regensburg, Germany

    Martin Schecklmann

  2. Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, Goethe-University Frankfurt, Frankfurt, Germany

    Christina Schwenck & Christine Freitag

  3. Department of Child and Adolescent Psychiatry, Psychosomatics and Psychotherapy, University Hospital of Würzburg, Würzburg, Germany

    Regina Taurines, Andreas Warnke, Manfred Gerlach & Marcel Romanos

Authors
  1. Martin Schecklmann
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Christina Schwenck
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Regina Taurines
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Christine Freitag
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Andreas Warnke
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Manfred Gerlach
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Marcel Romanos
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Martin Schecklmann.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Schecklmann, M., Schwenck, C., Taurines, R. et al. A systematic review on olfaction in child and adolescent psychiatric disorders. J Neural Transm 120, 121–130 (2013). https://doi.org/10.1007/s00702-012-0855-2

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00702-012-0855-2

Keywords

  • Obsessive–compulsive disorder
  • Attention deficit hyperactivity disorder
  • Schizophrenia
  • Autism
  • Olfaction
  • Dopamine
  • Review