Skip to main content
Top
Published in: BMC Psychiatry 1/2018

Open Access 01-12-2018 | Research article

Olfactory impairment in first-episode schizophrenia: a case-control study, and sex dimorphism in the relationship between olfactory impairment and psychotic symptoms

Authors: Xiacan Chen, Jiajun Xu, Bin Li, Wanjun Guo, Jun Zhang, Junmei Hu

Published in: BMC Psychiatry | Issue 1/2018

Login to get access

Abstract

Background

A body of studies has focused on the olfactory impairment among people with schizophrenia. The effect of sex on this relationship has attracted the attention of researchers. These issues have not been studied much in Chinese schizophrenia patients.

Methods

We conducted a case-control study of 110 first-episode antipsychotic medicine naïve schizophrenia patients aged 18–35 years and 110 controls, matched by age and sex. Odour threshold, discrimination and identification were assessed by the “Sniffin’ Sticks” test. Psychotic symptoms were assessed by the Positive and Negative Syndrome Scale (PANSS).

Results

The odour threshold, discrimination and identification scores of patients with schizophrenia were significantly lower than those of the healthy control group. The difference in identification score had statistical significance between male and female patients with schizophrenia (t = − 2.45, P < 0.05). Controlling for confounding factor, in male schizophrenia participants, the negative subscale score was significantly and inversely correlated with the discrimination (γ = − 0.37, p < 0.008), identification (γ = − 0.45, p < 0.008) and TDI (γ = − 0.50, p < 0.008) scores; the general psychopathology subscale score was inversely and significantly correlated with the identification (γ = − 0.47, p < 0.008) and TDI (γ = − 0.41, p < 0.008) scores. For female schizophrenia patients, positive and general psychopathology subscale scores had a significant inverse correlation with the identification score (positive: γ = − 0.47, p < 0.008; general psychopathology: γ = − 0.42, p < 0.008).

Conclusions

Controlling for confounder, negative symptoms were related to impaired odour discrimination and identification in male schizophrenia patients, while positive symptoms were correlated with impaired odour identification in female schizophrenia patients. This sex dimorphism could provide useful information for future studies aiming to finding biomarkers of schizophrenia.
Literature
1.
go back to reference Kahn RS, Keefe RSE. Schizophrenia is a cognitive illness: time for a change in focus. Jama Psychiatry. 2013;70(10):1107.CrossRefPubMed Kahn RS, Keefe RSE. Schizophrenia is a cognitive illness: time for a change in focus. Jama Psychiatry. 2013;70(10):1107.CrossRefPubMed
2.
3.
go back to reference Nolte J, S J. The human brain: an introduction to its functional anatomy. 6th ed. Philadelphia: Mosby; 2008. Nolte J, S J. The human brain: an introduction to its functional anatomy. 6th ed. Philadelphia: Mosby; 2008.
4.
go back to reference Ugur T, Weisbrod M, Franzek E, Pfuller U, Sauer H. Olfactory impairment in monozygotic twins discordant for schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2005;255(2):94–8.CrossRefPubMed Ugur T, Weisbrod M, Franzek E, Pfuller U, Sauer H. Olfactory impairment in monozygotic twins discordant for schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2005;255(2):94–8.CrossRefPubMed
5.
go back to reference Ishizuka K, Tajinda K, Colantuoni C, Morita M, Winicki J, Le C, Lin S, Schretlen D, Sawa A, Cascella NG. Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania smell identification test. Neurosci Res. 2010;66(1):106–10.CrossRefPubMed Ishizuka K, Tajinda K, Colantuoni C, Morita M, Winicki J, Le C, Lin S, Schretlen D, Sawa A, Cascella NG. Negative symptoms of schizophrenia correlate with impairment on the University of Pennsylvania smell identification test. Neurosci Res. 2010;66(1):106–10.CrossRefPubMed
6.
go back to reference Amsterdam JD, Settle RG, Doty RL, Abelman E, Winokur A. Taste and smell perception in depression. Biol Psychiatry. 1987;22(12):1481–5.CrossRefPubMed Amsterdam JD, Settle RG, Doty RL, Abelman E, Winokur A. Taste and smell perception in depression. Biol Psychiatry. 1987;22(12):1481–5.CrossRefPubMed
7.
go back to reference Rupp CI, Fleischhacker WW, Kemmler G, Oberbauer H, Scholtz AW, Wanko C, Hinterhuber H. Various bilateral olfactory deficits in male patients with schizophrenia. Schizophr Bull. 2005;31(1):155–65.CrossRefPubMed Rupp CI, Fleischhacker WW, Kemmler G, Oberbauer H, Scholtz AW, Wanko C, Hinterhuber H. Various bilateral olfactory deficits in male patients with schizophrenia. Schizophr Bull. 2005;31(1):155–65.CrossRefPubMed
8.
go back to reference Nguyen AD, Shenton ME, Levitt JJ. Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harv Rev Psychiatry. 2010;18(5):279–92.CrossRefPubMed Nguyen AD, Shenton ME, Levitt JJ. Olfactory dysfunction in schizophrenia: a review of neuroanatomy and psychophysiological measurements. Harv Rev Psychiatry. 2010;18(5):279–92.CrossRefPubMed
9.
go back to reference Pelka-Wysiecka J, Wronski M, Bienkowski P, Murawiec S, Samochowiec A, Samochowiec J. Odors identification differences in deficit and nondeficit schizophrenia. Pharmacol Rep. 2016;68(2):390–5.CrossRefPubMed Pelka-Wysiecka J, Wronski M, Bienkowski P, Murawiec S, Samochowiec A, Samochowiec J. Odors identification differences in deficit and nondeficit schizophrenia. Pharmacol Rep. 2016;68(2):390–5.CrossRefPubMed
10.
go back to reference Cohen AS, Brown LA, Auster TL. Olfaction, “olfiction”, and the schizophrenia-spectrum: an updated meta-analysis on identification and acuity. Schizophr Res. 2012;135(1–3):152–7.CrossRefPubMed Cohen AS, Brown LA, Auster TL. Olfaction, “olfiction”, and the schizophrenia-spectrum: an updated meta-analysis on identification and acuity. Schizophr Res. 2012;135(1–3):152–7.CrossRefPubMed
11.
go back to reference Hummel T, Kobal G, Gudziol H, Mackaysim A. 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. 2007;264(3):237–43.CrossRefPubMed Hummel T, Kobal G, Gudziol H, Mackaysim A. 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. 2007;264(3):237–43.CrossRefPubMed
12.
go back to reference Malaspina D, Goetz R, Keller A, Messinger JW, Bruder G, Goetz D, Opler M, Harlap S, Harkavy-Friedman J, Antonius D. Olfactory processing, sex effects and heterogeneity in schizophrenia. Schizophr Res. 2012;135(1–3):144–51.CrossRefPubMed Malaspina D, Goetz R, Keller A, Messinger JW, Bruder G, Goetz D, Opler M, Harlap S, Harkavy-Friedman J, Antonius D. Olfactory processing, sex effects and heterogeneity in schizophrenia. Schizophr Res. 2012;135(1–3):144–51.CrossRefPubMed
13.
go back to reference Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL. Olfactory dysfunction in schizophrenia : a qualitative and quantitative review. Neuropsychopharmacol Official Publ Am Coll europsychopharmacol. 1999;21(3):325–40.CrossRef Moberg PJ, Agrin R, Gur RE, Gur RC, Turetsky BI, Doty RL. Olfactory dysfunction in schizophrenia : a qualitative and quantitative review. Neuropsychopharmacol Official Publ Am Coll europsychopharmacol. 1999;21(3):325–40.CrossRef
14.
go back to reference Andia AM, Zisook S, Heaton RK, Hesselink J, Jernigan T, Kuck J, Morganville J, Braff DL. Gender differences in schizophrenia. J Nerv Ment Dis. 1995;183(8):522–8.CrossRefPubMed Andia AM, Zisook S, Heaton RK, Hesselink J, Jernigan T, Kuck J, Morganville J, Braff DL. Gender differences in schizophrenia. J Nerv Ment Dis. 1995;183(8):522–8.CrossRefPubMed
15.
go back to reference Ochoa S, Usall J, Cobo J, Labad X, Kulkarni J. Gender differences in schizophrenia and first-episode psychosis: a comprehensive literature review. Schizophrenia Res Treat. 2012;2012:916198. Ochoa S, Usall J, Cobo J, Labad X, Kulkarni J. Gender differences in schizophrenia and first-episode psychosis: a comprehensive literature review. Schizophrenia Res Treat. 2012;2012:916198.
16.
go back to reference Crow TJ, Chance SA, Priddle TH, Radua J, James AC. Laterality interacts with sex across the schizophrenia/bipolarity continuum: an interpretation of meta-analyses of structural MRI. Psychiatry Res. 2013;210(3):1232–44.CrossRefPubMed Crow TJ, Chance SA, Priddle TH, Radua J, James AC. Laterality interacts with sex across the schizophrenia/bipolarity continuum: an interpretation of meta-analyses of structural MRI. Psychiatry Res. 2013;210(3):1232–44.CrossRefPubMed
17.
go back to reference Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011;35(3):565–72.CrossRefPubMed Beery AK, Zucker I. Sex bias in neuroscience and biomedical research. Neurosci Biobehav Rev. 2011;35(3):565–72.CrossRefPubMed
18.
go back to reference Good KP, Leslie RA, McGlone J, Milliken HI, Kopala LC. Sex differences in olfactory function in young patients with psychotic disorders. Schizophr Res. 2007;97(1–3):97–102.CrossRefPubMed Good KP, Leslie RA, McGlone J, Milliken HI, Kopala LC. Sex differences in olfactory function in young patients with psychotic disorders. Schizophr Res. 2007;97(1–3):97–102.CrossRefPubMed
19.
go back to reference Sorokowska A, Schriever VA, Gudziol V, Hummel C, Hähner A, Iannilli E, Sinding C, Aziz M, Seo HS, Negoias S. Changes of olfactory abilities in relation to age: odor identification in more than 1400 people aged 4 to 80 years. Eur Arch Otorhinolaryngol. 2015;272(8):1937–44.CrossRefPubMed Sorokowska A, Schriever VA, Gudziol V, Hummel C, Hähner A, Iannilli E, Sinding C, Aziz M, Seo HS, Negoias S. Changes of olfactory abilities in relation to age: odor identification in more than 1400 people aged 4 to 80 years. Eur Arch Otorhinolaryngol. 2015;272(8):1937–44.CrossRefPubMed
20.
go back to reference Kay SR, Opler LA, Lindenmayer JP. Reliability and validity of the positive and negative syndrome scale for schizophrenics. Psychiatry Res. 1988;23(1):99–110.CrossRefPubMed Kay SR, Opler LA, Lindenmayer JP. Reliability and validity of the positive and negative syndrome scale for schizophrenics. Psychiatry Res. 1988;23(1):99–110.CrossRefPubMed
21.
go back to reference Kobal G, Klimek L, Wolfensberger M, Gudziol H, Temmel A, Owen CM, Seeber H, Pauli E, Hummel T. Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol. 2000;257(4):205–11.CrossRefPubMed Kobal G, Klimek L, Wolfensberger M, Gudziol H, Temmel A, Owen CM, Seeber H, Pauli E, Hummel T. Multicenter investigation of 1,036 subjects using a standardized method for the assessment of olfactory function combining tests of odor identification, odor discrimination, and olfactory thresholds. Eur Arch Otorhinolaryngol. 2000;257(4):205–11.CrossRefPubMed
22.
go back to reference Kobal G, Hummel T, Sekinger B, Barz S, Roscher S, Wolf S. “Sniffin’ sticks”: screening of olfactory performance. Rhinology. 1996;34(4):222–6.PubMed Kobal G, Hummel T, Sekinger B, Barz S, Roscher S, Wolf S. “Sniffin’ sticks”: screening of olfactory performance. Rhinology. 1996;34(4):222–6.PubMed
23.
go back to reference Hurwitz T, Kopala L, Clark C, Jones B. Olfactory deficits in schizophrenia. Biol Psychiatry. 1988;23(2):123–8.CrossRefPubMed Hurwitz T, Kopala L, Clark C, Jones B. Olfactory deficits in schizophrenia. Biol Psychiatry. 1988;23(2):123–8.CrossRefPubMed
24.
go back to reference Zou LQ, Zhou HY, Lui SSY, Wang Y, Wang Y, Gan J, Zhu XZ, Cheung EFC, Chan RCK. Olfactory identification deficit and its relationship with hedonic traits in patients with first-episode schizophrenia and individuals with schizotypy. Prog Neuro-Psychopharmacol Biol Psychiatry. 2018;83:137–41.CrossRef Zou LQ, Zhou HY, Lui SSY, Wang Y, Wang Y, Gan J, Zhu XZ, Cheung EFC, Chan RCK. Olfactory identification deficit and its relationship with hedonic traits in patients with first-episode schizophrenia and individuals with schizotypy. Prog Neuro-Psychopharmacol Biol Psychiatry. 2018;83:137–41.CrossRef
25.
go back to reference Good KP, Whitehorn D, Rui Q, Milliken H, Kopala LC. Olfactory identification deficits in first-episode psychosis may predict patients at risk for persistent negative and disorganized or cognitive symptoms. Am J Psychiatr. 2006;163(163):932–3.CrossRefPubMed Good KP, Whitehorn D, Rui Q, Milliken H, Kopala LC. Olfactory identification deficits in first-episode psychosis may predict patients at risk for persistent negative and disorganized or cognitive symptoms. Am J Psychiatr. 2006;163(163):932–3.CrossRefPubMed
26.
go back to reference Good KP, Tibbo P, Milliken H, Whitehorn D, Alexiadis M, Robertson N, Kopala LC. An investigation of a possible relationship between olfactory identification deficits at first episode and four-year outcomes in patients with psychosis. Schizophr Res. 2010;124(1–3):60–5.CrossRefPubMed Good KP, Tibbo P, Milliken H, Whitehorn D, Alexiadis M, Robertson N, Kopala LC. An investigation of a possible relationship between olfactory identification deficits at first episode and four-year outcomes in patients with psychosis. Schizophr Res. 2010;124(1–3):60–5.CrossRefPubMed
27.
go back to reference Highley JR, DeLisi LE, Roberts N, Webb JA, Relja M, Razi K, Crow TJ. Sex-dependent effects of schizophrenia: an MRI study of gyral folding, and cortical and white matter volume. Psychiatry Res. 2003;124(1):11–23.CrossRefPubMed Highley JR, DeLisi LE, Roberts N, Webb JA, Relja M, Razi K, Crow TJ. Sex-dependent effects of schizophrenia: an MRI study of gyral folding, and cortical and white matter volume. Psychiatry Res. 2003;124(1):11–23.CrossRefPubMed
28.
go back to reference Abel KM, Drake R, Goldstein JM. Sex differences in schizophrenia. Int Rev Psychiatry. 2010;22(5):417–28.CrossRefPubMed Abel KM, Drake R, Goldstein JM. Sex differences in schizophrenia. Int Rev Psychiatry. 2010;22(5):417–28.CrossRefPubMed
29.
go back to reference Urban M, Rabe-Jablonska J. Olfactory dysfunctions in patients with schizophrenia. Psychiatr Pol. 2007;41(4):503–12.PubMed Urban M, Rabe-Jablonska J. Olfactory dysfunctions in patients with schizophrenia. Psychiatr Pol. 2007;41(4):503–12.PubMed
30.
go back to reference Kamath V, Lasutschinkow P, Ishizuka K, Sawa A. Olfactory functioning in first-episode psychosis. Schizophr Bull. 2017;44(3):672–80. Kamath V, Lasutschinkow P, Ishizuka K, Sawa A. Olfactory functioning in first-episode psychosis. Schizophr Bull. 2017;44(3):672–80.
31.
go back to reference Rupp CI, Fleischhacker WW, Kemmler G, Kremser C, Bilder RM, Mechtcheriakov S, Szeszko PR, Walch T, Scholtz AW, Klimbacher M, et al. Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia. Schizophr Res. 2005;74(2–3):149–61.CrossRefPubMed Rupp CI, Fleischhacker WW, Kemmler G, Kremser C, Bilder RM, Mechtcheriakov S, Szeszko PR, Walch T, Scholtz AW, Klimbacher M, et al. Olfactory functions and volumetric measures of orbitofrontal and limbic regions in schizophrenia. Schizophr Res. 2005;74(2–3):149–61.CrossRefPubMed
32.
go back to reference Rahm C, Liberg B, Reckless G, Ousdal O, Melle I, Andreassen OA, Agartz I. Negative symptoms in schizophrenia show association with amygdala volumes and neural activation during affective processing. Acta Neuropsychiatrica. 2015;27(4):213–20.CrossRefPubMed Rahm C, Liberg B, Reckless G, Ousdal O, Melle I, Andreassen OA, Agartz I. Negative symptoms in schizophrenia show association with amygdala volumes and neural activation during affective processing. Acta Neuropsychiatrica. 2015;27(4):213–20.CrossRefPubMed
33.
go back to reference Gur RE, Kohler C, Turetsky BI, Siegel SJ, Kanes SJ, Bilker WB, Brennan AR, Gur RC. A sexually dimorphic ratio of orbitofrontal to amygdala volume is altered in schizophrenia. Biol Psychiatry. 2004;55(5):512–7.CrossRefPubMed Gur RE, Kohler C, Turetsky BI, Siegel SJ, Kanes SJ, Bilker WB, Brennan AR, Gur RC. A sexually dimorphic ratio of orbitofrontal to amygdala volume is altered in schizophrenia. Biol Psychiatry. 2004;55(5):512–7.CrossRefPubMed
34.
go back to reference Semkovska M, Bedard MA, Stip E. Hypofrontality and negative symptoms in schizophrenia: synthesis of anatomic and neuropsychological knowledge and ecological perspectives. Encephale. 2001;27(5):405–15.PubMed Semkovska M, Bedard MA, Stip E. Hypofrontality and negative symptoms in schizophrenia: synthesis of anatomic and neuropsychological knowledge and ecological perspectives. Encephale. 2001;27(5):405–15.PubMed
35.
go back to reference Shinto AS, Kamaleshwaran KK, Srinivasan D, Paranthaman S, Selvaraj K, Pranesh MB, Lakshminarayanan GN, Prakash B. “Hyperfrontality” as seen on FDG PET in unmedicated schizophrenia patients with positive symptoms. Clin Nucl Med. 2014;39(8):694–7.CrossRefPubMed Shinto AS, Kamaleshwaran KK, Srinivasan D, Paranthaman S, Selvaraj K, Pranesh MB, Lakshminarayanan GN, Prakash B. “Hyperfrontality” as seen on FDG PET in unmedicated schizophrenia patients with positive symptoms. Clin Nucl Med. 2014;39(8):694–7.CrossRefPubMed
36.
go back to reference Oliveira-Pinto AV, Santos RM, Coutinho RA, Oliveira LM, Santos GB, Alho AT, Leite RE, Farfel JM, Suemoto CK, Grinberg LT, et al. Sexual dimorphism in the human olfactory bulb: females have more neurons and glial cells than males. PLoS One. 2014;9(11):e111733.CrossRefPubMedPubMedCentral Oliveira-Pinto AV, Santos RM, Coutinho RA, Oliveira LM, Santos GB, Alho AT, Leite RE, Farfel JM, Suemoto CK, Grinberg LT, et al. Sexual dimorphism in the human olfactory bulb: females have more neurons and glial cells than males. PLoS One. 2014;9(11):e111733.CrossRefPubMedPubMedCentral
37.
go back to reference Quarmley M, Moberg PJ, Mechanic-Hamilton D, Kabadi S, Arnold SE, Wolk DA, Roalf DR. Odor identification screening improves diagnostic classification in incipient Alzheimer's disease. J Alzheimers Dis Jad. 2016;55(4):1497–507. Quarmley M, Moberg PJ, Mechanic-Hamilton D, Kabadi S, Arnold SE, Wolk DA, Roalf DR. Odor identification screening improves diagnostic classification in incipient Alzheimer's disease. J Alzheimers Dis Jad. 2016;55(4):1497–507.
Metadata
Title
Olfactory impairment in first-episode schizophrenia: a case-control study, and sex dimorphism in the relationship between olfactory impairment and psychotic symptoms
Authors
Xiacan Chen
Jiajun Xu
Bin Li
Wanjun Guo
Jun Zhang
Junmei Hu
Publication date
01-12-2018
Publisher
BioMed Central
Published in
BMC Psychiatry / Issue 1/2018
Electronic ISSN: 1471-244X
DOI
https://doi.org/10.1186/s12888-018-1786-8

Other articles of this Issue 1/2018

BMC Psychiatry 1/2018 Go to the issue