Hostname: page-component-8448b6f56d-xtgtn Total loading time: 0 Render date: 2024-04-23T09:30:50.857Z Has data issue: false hasContentIssue false
  • English
  • Français

The olfactory deficits of depressed patients are restored after remission with venlafaxine treatment

Published online by Cambridge University Press:  22 October 2020

Romain Colle ,
Khalil El Asmar ,
Céline Verstuyft ,
Pierre-Marie Lledo ,
Françoise Lazarini ,
Kenneth Chappell ,
Eric Deflesselle ,
Abd El Kader Ait Tayeb ,
Bruno Falissard  and
Emmanuelle Duron
...Show all authors
Romain Colle*
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service Hospitalo-Universitaire de Psychiatrie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Khalil El Asmar
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France
Céline Verstuyft
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service de Génétique moléculaire, Pharmacogénétique et Hormonologie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Pierre-Marie Lledo
Affiliation:
Unité Perception et Mémoire, Institut Pasteur, CNRS UMR3571, Paris, F-75015, France
Françoise Lazarini
Affiliation:
Service de Génétique moléculaire, Pharmacogénétique et Hormonologie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Kenneth Chappell
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France
Eric Deflesselle
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France
Abd El Kader Ait Tayeb
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service Hospitalo-Universitaire de Psychiatrie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Bruno Falissard
Affiliation:
Département de Biostatistiques, Université Paris-Sud, Hôpital Paul Brousse, Assistance Publique Hôpitaux de Paris, Villejuif 94400, France
Emmanuelle Duron
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France
Samuel Rotenberg
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service Hospitalo-Universitaire de Psychiatrie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Jean-Francois Costemale-Lacoste
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France
Denis J. David
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Univ. Paris-Sud, Fac. Pharmacie, Inserm, Université Paris-Saclay, Chatenay Malabry 92290, France
Florence Gressier
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service Hospitalo-Universitaire de Psychiatrie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Alain M. Gardier
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Univ. Paris-Sud, Fac. Pharmacie, Inserm, Université Paris-Saclay, Chatenay Malabry 92290, France
Thomas Hummel
Affiliation:
Department of Otorhinolaryngology, Smell and Taste Clinic, Dresden, TU, Germany
Laurent Becquemont
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Centre de recherche clinique, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
Emmanuelle Corruble
Affiliation:
Equipe Moods, INSERM UMR-1178, CESP, Université Paris-Sud, Faculté de Médecine Paris-Sud, Le Kremlin Bicêtre, F-94276, France Service Hospitalo-Universitaire de Psychiatrie, Assistance Publique-Hôpitaux de Paris, Hôpitaux Universitaires Paris-Sud, Hôpital de Bicêtre, Le Kremlin Bicêtre, F-94275, France
*
Author for correspondence: Romain Colle, E-mail: romaincolle@hotmail.com
Get access Rights & Permissions [Opens in a new window]

Abstract

Background

It is unclear whether olfactory deficits improve after remission in depressed patients. Therefore, we aimed to assess in drug-free patients the olfactory performance of patients with major depressive episodes (MDE) and its change after antidepressant treatment.

Methods

In the DEP-ARREST-CLIN study, 69 drug-free patients with a current MDE in the context of major depressive disorder (MDD) were assessed for their olfactory performances and depression severity, before and after 1 (M1) and 3 (M3) months of venlafaxine antidepressant treatment. They were compared to 32 age- and sex-matched healthy controls (HCs). Olfaction was assessed with a psychophysical test, the Sniffin’ Sticks test (Threshold: T score; Discrimination: D score; Identification: I score; total score: T + D + I = TDI score) and Pleasantness (pleasantness score: p score; neutral score: N score; unpleasantness score: U score).

Results

As compared to HCs, depressed patients had lower TDI olfactory scores [mean (s.d.) 30.0(4.5) v. 33.3(4.2), p < 0.001], T scores [5.6(2.6) v. 7.4(2.6), p < 0.01], p scores [7.5(3.0) v. 9.8(2.8), p < 0.001)] and higher N scores [3.5(2.6) v. 2.1(1.8), p < 0.01]. T, p and N scores at baseline were independent from depression and anhedonia severity. After venlafaxine treatment, significant increases of T scores [M1: 7.0(2.6) and M3: 6.8(3.1), p < 0.01] and p scores [M1: 8.1(3.0) and M3: 8.4(3.3), p < 0.05] were evidenced, in remitters only (T: p < 0.01; P: p < 0.01). Olfaction improvement was mediated by depression improvement.

Conclusions

The olfactory signature of MDE is restored after venlafaxine treatment. This olfaction improvement is mediated by depression improvement.

Keywords

Antidepressantsmajor depressionmajor depressive disorderolfactionolfactory pleasantnessolfactory sensitivityolfactory thresholdremission
Type
Original Article
Information
Psychological Medicine , Volume 52 , Issue 11 , August 2022 , pp. 2062 - 2070
Copyright
Copyright © The Author(s), 2020. Published by Cambridge University Press

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

Ajmani, G. S., Suh, H. H., Wroblewski, K. E., & Pinto, J. M. (2017). Smoking and olfactory dysfunction: A systematic literature review and meta-analysis. The Laryngoscope, 127, 1753–1761. doi: 10.1002/lary.26558CrossRefGoogle ScholarPubMed
Al Ain, S., Poupon, D., Hetu, S., Mercier, N., Steffener, J., & Frasnelli, J. (2019). Smell training improves olfactory function and alters brain structure. NeuroImage, 189, 45–54. doi: 10.1016/j.neuroimage.2019.01.008CrossRefGoogle ScholarPubMed
Albrecht, J., Anzinger, A., Kopietz, R., Schopf, V., Kleemann, A. M., Pollatos, O., & Wiesmann, M. (2008). Test-retest reliability of the olfactory detection threshold test of the Sniffin’ sticks. Chemical Senses, 33, 461–7. doi: 10.1093/chemse/bjn013CrossRefGoogle ScholarPubMed
Atanasova, B., El-Hage, W., Chabanet, C., Gaillard, P., Belzung, C., & Camus, V. (2010). Olfactory anhedonia and negative olfactory alliesthesia in depressed patients. Psychiatry Research, 176, 190–6. doi: 10.1016/j.psychres.2008.11.016CrossRefGoogle ScholarPubMed
Bensafi, M., Sobel, N., & Khan, R. M. (2007). Hedonic-specific activity in piriform cortex during odor imagery mimics that during odor perception. Journal of Neurophysiology, 98, 3254–62. doi: 10.1152/jn.00349.2007CrossRefGoogle ScholarPubMed
Berlim, M. T., & Turecki, G. (2007). Definition, assessment, and staging of treatment-resistant refractory major depression: A review of current concepts and methods. Canadian Journal of Psychiatry. Revue canadienne de Psychiatrie, 52, 46–54. doi: 10.1177/070674370705200108CrossRefGoogle ScholarPubMed
Birte-Antina, W., Ilona, C., Antje, H., & Thomas, H. (2018). Olfactory training with older people. International Journal of Geriatric Psychiatry, 33, 212–220. doi: 10.1002/gps.4725CrossRefGoogle ScholarPubMed
Borgmann-Winter, K. E., Rawson, N. E., Wang, H. Y., Wang, H., Macdonald, M. L., Ozdener, M. H., … Hahn, C. G. (2009). Human olfactory epithelial cells generated in vitro express diverse neuronal characteristics. Neuroscience, 158, 642–53. doi: 10.1016/j.neuroscience.2008.09.059CrossRefGoogle ScholarPubMed
Bushdid, C., Magnasco, M. O., Vosshall, L. B., & Keller, A. (2014). Humans can discriminate more than 1 trillion olfactory stimuli. Science, 343, 1370–2. doi: 10.1126/science.1249168CrossRefGoogle ScholarPubMed
Chen, B., Klarmann, R., Israel, M., Ning, Y., Colle, R., & Hummel, T. (2019). Difference of olfactory deficit in patients with acute episode of schizophrenia and major depressive episode. Schizophrenia Research, 212, 99–106.CrossRefGoogle ScholarPubMed
Cheng, K., Li, J., Yang, D., Yang, Y., Rao, C., Zhang, S., … Xie, P. (2016). 2D-gel based proteomics unravels neurogenesis and energetic metabolism dysfunction of the olfactory bulb in CUMS rat model. Behavioural Brain Research, 313, 302–309. doi: 10.1016/j.bbr.2016.05.026CrossRefGoogle ScholarPubMed
Clepce, M., Gossler, A., Reich, K., Kornhuber, J., & Thuerauf, N. (2010). The relation between depression, anhedonia and olfactory hedonic estimates—a pilot study in major depression. Neuroscience Letters, 471, 139–43. doi: 10.1016/j.neulet.2010.01.027CrossRefGoogle Scholar
Croy, I., & Hummel, T. (2017). Olfaction as a marker for depression. Journal of Neurology, 264, 631–638. doi: 10.1007/s00415-016-8227-8.CrossRefGoogle ScholarPubMed
Croy, I., Symmank, A., Schellong, J., Hummel, C., Gerber, J., Joraschky, P., & Hummel, T. (2014). Olfaction as a marker for depression in humans. Journal of Affective Disorders, 160, 80–6. doi: 10.1016/j.jad.2013.12.026CrossRefGoogle ScholarPubMed
Doty, R. L., McKeown, D. A., Lee, W. W., & Shaman, P. (1995). A study of the test-retest reliability of ten olfactory tests. Chemical Senses, 20, 645–56. doi: 10.1093/chemse/20.6.645CrossRefGoogle ScholarPubMed
Gaines, A. (2013). Chapter 13: Olfactory disorders. American Journal of Rhinology & Allergy, 27(Suppl 1), S45–7. doi: 10.2500/ajra.2013.27.3898CrossRefGoogle ScholarPubMed
Gorwood, P., Corruble, E., Falissard, B., & Goodwin, G. M. (2008). Toxic effects of depression on brain function: Impairment of delayed recall and the cumulative length of depressive disorder in a large sample of depressed outpatients. The American Journal of Psychiatry, 165, 731–9. doi: 10.1176/appi.ajp.2008.07040574CrossRefGoogle 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. Biological Psychiatry, 35, 798–802.CrossRefGoogle ScholarPubMed
Hamilton, M. (1960). A rating scale for depression. Journal of Neurology, Neurosurgery, and Psychiatry, 23, 56–62.CrossRefGoogle ScholarPubMed
Harless, L., & Liang, J. (2016). Pharmacologic treatment for postviral olfactory dysfunction: A systematic review. International Forum of Allergy & Rhinology, 6, 760–7. doi: 10.1002/alr.21727CrossRefGoogle ScholarPubMed
Hedner, M., Larsson, M., Arnold, N., Zucco, G. M., & Hummel, T. (2010). Cognitive factors in odor detection, odor discrimination, and odor identification tasks. Journal of Clinical and Experimental Neuropsychology, 32, 1062–7. doi: 10.1080/13803391003683070CrossRefGoogle ScholarPubMed
Hennings, J. M., Owashi, T., Binder, E. B., Horstmann, S., Menke, A., Kloiber, S., … Lucae, S. (2009). Clinical characteristics and treatment outcome in a representative sample of depressed inpatients – findings from the Munich Antidepressant Response Signature (MARS) project. Journal of Psychiatric Research, 43, 215–29. doi: 10.1016/j.jpsychires.2008.05.002CrossRefGoogle Scholar
Horio, N., Murata, K., Yoshikawa, K., Yoshihara, Y., & Touhara, K. (2019). Contribution of individual olfactory receptors to odor-induced attractive or aversive behavior in mice. Nature Communications, 10, 209. doi: 10.1038/s41467-018-07940-1CrossRefGoogle ScholarPubMed
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 3000 subjects. European Archives of Oto-Rhino-Laryngology : Official Journal of the European Federation of Oto-Rhino-Laryngological Societies, 264, 237–43. doi: 10.1007/s00405-006-0173-0CrossRefGoogle Scholar
Hummel, T., Sekinger, B., Wolf, S. R., Pauli, E., & Kobal, G. (1997). ‘Sniffin’ sticks’: Olfactory performance assessed by the combined testing of odor identification, odor discrimination and olfactory threshold. Chemical Senses, 22, 39–52.CrossRefGoogle ScholarPubMed
Kamath, V., Paksarian, D., Cui, L., Moberg, P. J., Turetsky, B. I., & Merikangas, K. R. (2018). Olfactory processing in bipolar disorder, major depression, and anxiety. Bipolar Disorders, 20, 547–555. doi: 10.1111/bdi.12625CrossRefGoogle ScholarPubMed
Kienke, A. S., & Rosenbaum, J. F. (2000). Efficacy of venlafaxine in the treatment of severe depression. Depression and Anxiety, 12(Suppl 1), 50–4. doi: 10.1002/1520-6394(2000)12:1+<50::AID-DA6>3.0.CO;2-43.0.CO;2-4>CrossRefGoogle ScholarPubMed
Kohli, P., Soler, Z. M., Nguyen, S. A., Muus, J. S., & Schlosser, R. J. (2016). The association between olfaction and depression: A systematic review. Chemical Senses, 41, 479–86. doi: 10.1093/chemse/bjw061CrossRefGoogle ScholarPubMed
Kopala, L. C., Good, K. P., & Honer, W. G. (1994). Olfactory hallucinations and olfactory identification ability in patients with schizophrenia and other psychiatric disorders. Schizophrenia Research, 12, 205–11.CrossRefGoogle ScholarPubMed
Lapid, H., Shushan, S., Plotkin, A., Voet, H., Roth, Y., Hummel, T., … Sobel, N. (2011). Neural activity at the human olfactory epithelium reflects olfactory perception. Nature Neuroscience, 14, 1455–61. doi: 10.1038/nn.2926CrossRefGoogle ScholarPubMed
Li, Q., Yang, D., Wang, J., Liu, L., Feng, G., Li, J., … Li, Z. (2015). Reduced amount of olfactory receptor neurons in the rat model of depression. Neuroscience Letters, 603, 48–54. doi: 10.1016/j.neulet.2015.07.007CrossRefGoogle ScholarPubMed
Lombion-Pouthier, S., Vandel, P., Nezelof, S., Haffen, E., & Millot, J. L. (2006). Odor perception in patients with mood disorders. Journal of Affective Disorders, 90, 187–91. doi: 10.1016/j.jad.2005.11.012CrossRefGoogle ScholarPubMed
Miller, B. R., & Hen, R. (2015). The current state of the neurogenic theory of depression and anxiety. Current Opinion in Neurobiology, 30C, 51–58. doi: 10.1016/j.conb.2014.08.012CrossRefGoogle Scholar
Mokdad, A. H., Forouzanfar, M. H., Daoud, F., Mokdad, A. A., El Bcheraoui, C., Moradi-Lakeh, M., … Murray, C. J. (2016). Global burden of diseases, injuries, and risk factors for young people's health during 1990-2013: A systematic analysis for the global burden of disease study 2013. Lancet, 387, 2383–401. doi: 10.1016/S0140-6736(16)00648-6CrossRefGoogle ScholarPubMed
Moller, H. J. (2008). Outcomes in major depressive disorder: The evolving concept of remission and its implications for treatment. The World Journal of Biological Psychiatry: the Official Journal of the World Federation of Societies of Biological Psychiatry, 9, 102–14. doi: 10.1080/15622970801981606CrossRefGoogle ScholarPubMed
Naudin, M., El-Hage, W., Gomes, M., Gaillard, P., Belzung, C., & Atanasova, B. (2012). State and trait olfactory markers of major depression. PloS One, 7, e46938. doi: 10.1371/journal.pone.0046938CrossRefGoogle ScholarPubMed
Negoias, S., Croy, I., Gerber, J., Puschmann, S., Petrowski, K., Joraschky, P., & Hummel, T. (2010). Reduced olfactory bulb volume and olfactory sensitivity in patients with acute major depression. Neuroscience, 169, 415–21. doi: 10.1016/j.neuroscience.2010.05.012CrossRefGoogle ScholarPubMed
Okamoto, A., Kuriyama, H., Watanabe, S., Aihara, Y., Tadai, T., Imanishi, J., & Fukui, K. (2005). The effect of aromatherapy massage on mild depression: A pilot study. Psychiatry and Clinical Neurosciences, 59, 363. doi: 10.1111/j.1440-1819.2005.01385.xCrossRefGoogle ScholarPubMed
Pause, B. M., Miranda, A., Goder, R., Aldenhoff, J. B., & Ferstl, R. (2001). Reduced olfactory performance in patients with major depression. Journal of Psychiatric Research, 35, 271–7.CrossRefGoogle ScholarPubMed
Pentzek, M., Grass-Kapanke, B., & Ihl, R. (2007). Odor identification in Alzheimer's disease and depression. Aging Clinical and Experimental Research, 19, 255–8.CrossRefGoogle ScholarPubMed
Pratt, L. A., Brody, D. J., & Gu, Q. (2011). Antidepressant use in persons aged 12 and over: United States, 2005-2008. NCHS Data Brief, 283, 1–8.Google Scholar
Rossi, M., Perez-Lloret, S., Millar Vernetti, P., Drucaroff, L., Costanzo, E., Ballesteros, D., … Merello, M. (2015). Olfactory dysfunction evaluation is not affected by comorbid depression in Parkinson's disease. Movement Disorders: Official Journal of the Movement Disorder Society, 30, 1275–9. doi: 10.1002/mds.26276CrossRefGoogle Scholar
Rottstadt, F., Han, P., Weidner, K., Schellong, J., Wolff-Stephan, S., Strauss, T., … Croy, I. (2018). Reduced olfactory bulb volume in depression—A structural moderator analysis. Human Brain Mapping, 39, 2573–2582. doi: 10.1002/hbm.24024.CrossRefGoogle ScholarPubMed
Rush, A. J., Kraemer, H. C., Sackeim, H. A., Fava, M., Trivedi, M. H., Frank, E., … Force, A. T. (2006). Report by the ACNP task force on response and remission in major depressive disorder. Neuropsychopharmacology: Official Publication of the American College of Neuropsychopharmacology, 31, 1841–53. doi: 10.1038/sj.npp.1301131.CrossRefGoogle ScholarPubMed
Scinska, A., Wrobel, E., Korkosz, A., Zatorski, P., Sienkiewicz-Jarosz, H., Lojkowska, W., … Kukwa, W. (2008). Depressive symptoms and olfactory function in older adults. Psychiatry and Clinical Neurosciences, 62, 450–6. doi: 10.1111/j.1440-1819.2008.01824.xCrossRefGoogle ScholarPubMed
Serby, M., Larson, P., & Kalkstein, D. (1990). Olfactory sense in psychoses. Biological Psychiatry, 28, 830.CrossRefGoogle ScholarPubMed
Sheehan, D. V., Lecrubier, Y., Sheehan, K. H., Amorim, P., Janavs, J., Weiller, E., … Dunbar, G. C. (1998). The Mini-International Neuropsychiatric Interview (M.I.N.I.): The development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. The Journal of Clinical Psychiatry, 59(Suppl 20), 22–33, quiz 34–57.Google ScholarPubMed
Siopi, E., Denizet, M., Gabellec, M. M., de Chaumont, F., Olivo-Marin, J. C., Guilloux, J. P., … Lazarini, F. (2016). Anxiety- and depression-like states lead to pronounced olfactory deficits and impaired adult neurogenesis in mice. The Journal of Neuroscience: the Official Journal of the Society for Neuroscience, 36, 518–31. doi: 10.1523/JNEUROSCI.2817-15.2016CrossRefGoogle ScholarPubMed
Snaith, R. P., Hamilton, M., Morley, S., Humayan, A., Hargreaves, D., & Trigwell, P. (1995). A scale for the assessment of hedonic tone the Snaith-Hamilton pleasure scale. The British Journal of Psychiatry: the Journal of Mental Science, 167, 99–103.CrossRefGoogle ScholarPubMed
Sorokowska, A., Albrecht, E., Haehner, A., & Hummel, T. (2015). Extended version of the “Sniffin’ Sticks” identification test: Test-retest reliability and validity. Journal of Neuroscience Methods, 243, 111–4. doi: 10.1016/j.jneumeth.2015.01.034CrossRefGoogle ScholarPubMed
Sorokowska, A., Drechsler, E., Karwowski, M., & Hummel, T. (2017). Effects of olfactory training: A meta-analysis. Rhinology, 55, 17–26. doi: 10.4193/Rhin16.195.CrossRefGoogle ScholarPubMed
Streiner, D. L., & Norman, G. R. (2011). Correction for multiple testing: Is there a resolution? Chest, 140, 16–18. doi: 10.1378/chest.11-0523CrossRefGoogle ScholarPubMed
Swiecicki, L., Zatorski, P., Bzinkowska, D., Sienkiewicz-Jarosz, H., Szyndler, J., & Scinska, A. (2009). Gustatory and olfactory function in patients with unipolar and bipolar depression. Progress in Neuro-Psychopharmacology & Biological Psychiatry, 33, 827–34. doi: 10.1016/j.pnpbp.2009.03.030CrossRefGoogle ScholarPubMed
Trivedi, M. H., Rush, A. J., Wisniewski, S. R., Nierenberg, A. A., Warden, D., Ritz, L., … Team, S. D. S. (2006). Evaluation of outcomes with citalopram for depression using measurement-based care in STAR*D: Implications for clinical practice. The American Journal of Psychiatry, 163, 28–40. doi: 10.1176/appi.ajp.163.1.28CrossRefGoogle ScholarPubMed
Villa, R. F., Ferrari, F., Bagini, L., Gorini, A., Brunello, N., & Tascedda, F. (2017). Mitochondrial energy metabolism of rat hippocampus after treatment with the antidepressants desipramine and fluoxetine. Neuropharmacology, 121, 30–38. doi: 10.1016/j.neuropharm.2017.04.025CrossRefGoogle ScholarPubMed
Warner, M. D., Peabody, C. A., & Csernansky, J. G. (1990). Olfactory functioning in schizophrenia and depression. Biological Psychiatry, 27, 457–8.CrossRefGoogle ScholarPubMed
Wechsler, D. (1987). Wechsler memory scale–revised. New York, Psychological Corp.Google Scholar
Yahiaoui-Doktor, M., Luck, T., Riedel-Heller, S. G., Loeffler, M., Wirkner, K., & Engel, C. (2019). Olfactory function is associated with cognitive performance: Results from the population-based LIFE-adult-study. Alzheimer's Research & Therapy, 11, 43. doi: 10.1186/s13195-019-0494-zCrossRefGoogle ScholarPubMed
Zucco, G. M., & Bollini, F. (2011). Odour recognition memory and odour identification in patients with mild and severe major depressive disorders. Psychiatry Research, 190, 217–20. doi: 10.1016/j.psychres.2011.08.025CrossRefGoogle ScholarPubMed
Zuccoli, G. S., Saia-Cereda, V. M., Nascimento, J. M., & Martins-de-Souza, D. (2017). The energy metabolism dysfunction in psychiatric disorders postmortem brains: Focus on proteomic evidence. Frontiers in Neuroscience, 11, 493. doi: 10.3389/fnins.2017.00493CrossRefGoogle ScholarPubMed
Supplementary material: File

Colle et al. supplementary material

Table S1 and Figures S1-S2

Download Colle et al. supplementary material(File)
File 187.9 KB