Hostname: page-component-586b7cd67f-rdxmf Total loading time: 0 Render date: 2024-11-29T07:16:40.317Z Has data issue: false hasContentIssue false

Odor sensitivity impairment: a behavioral marker of psychological distress?

Published online by Cambridge University Press:  27 September 2018

David C. Houghton*
Affiliation:
Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, South Carolina, USA Department of Psychological and Brain Sciences, Texas A&M University, College Station, Texas, USA
Samuel L. Howard
Affiliation:
Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, South Carolina, USA
Thomas W. Uhde
Affiliation:
Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, South Carolina, USA
Caitlin Paquet
Affiliation:
Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, South Carolina, USA
Rodney J. Schlosser
Affiliation:
Department of Otolaryngology Head and Neck Surgery, Medical University of South Carolina, Charleston, South Carolina, USA
Bernadette M. Cortese*
Affiliation:
Department of Psychiatry and Behavioral Sciences, Medical University of South Carolina, Charleston, South Carolina, USA
*
*Address for correspondence: Bernadette M. Cortese, PhD, Department of Psychiatry and Behavioral Sciences, The Medical University of South Carolina, 67 President Street, MSC 861, Charleston, SC 29425, USA. (Email: [email protected])

Abstract

Objective

Enhanced odor sensitivity, particularly toward threat-related cues, may be adaptive during periods of danger. Research also suggests that chronic psychological distress may lead to functional changes in the olfactory system that cause heightened sensitivity to odors. Yet, the association between self-reported odor sensitivity, objective odor detection, and affective psychopathology is currently unclear, and research suggests that persons with affective problems may only be sensitive to specific, threat-related odors.

Methods

The current study compared adults with self-reported odor sensitivity that was described as functionally impairing (OSI; n = 32) to those who reported odor sensitivity that was non-impairing (OS; n = 17) on affective variables as well as quantitative odor detection.

Results

Increased anxiety sensitivity, trait anxiety, depression, and life stress, even while controlling for comorbid anxiety and depressive disorders, was found for OSI compared to OS. While OSI, compared to OS, demonstrated only a trend increase in objective odor detection of a smoke-like, but not rose-like, odor, further analysis revealed that increased detection of that smoke-like odor was positively correlated with anxiety sensitivity.

Conclusion

These findings suggest that persons with various forms of psychological distress may find themselves significantly impaired by an intolerance of odors, but that self-reported odor sensitivity does not necessarily relate to enhanced odor detection ability. However, increased sensitivity to a smoke-like odor appears to be associated with sensitivity to aversive anxiogenic stimuli. Implications for the pathophysiology of fear- and anxiety-related disorders are discussed.

Type
Original Research
Copyright
© Cambridge University Press 2018 

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.)

Footnotes

Funding for this study was provided by NIMH Grant K01 MH090548 (BMC).

References

References:

McGann, JP. Poor human olfaction is a 19th-century myth. Science. 2017;356(6338). doi: 10.1126/science.aam7263 CrossRefGoogle Scholar
Sarafoleanu, C, Mella, C, Georgescu, M, Perederco C. The importance of the olfactory sense in the human behavior and evolution. J Med Life. 2009;2(2):196198.Google ScholarPubMed
Lukowiak, K, Martens, K, Rosenegger, D, Browning K, de Caigny P, Orr M. The perception of stress alters adaptive behaviors in Lymnaea stagnalis . J Exp Biol. 2008;211(Pt 11):17471756.CrossRefGoogle ScholarPubMed
Sung, KK, Jang, DP, Lee, S, Kim M, Lee SY, Kim YB, et al. Neural responses in rat brain during acute immobilization stress: a [F-18]FDG micro PET imaging study. Neuroimage. 2009;44(3):10741080.CrossRefGoogle Scholar
Jones, SV, Choi, DC, Davis, M, Ressler KJ. Learning-dependent structural plasticity in the adult olfactory pathway. J Neurosci. 2008;28(49):1310613111.CrossRefGoogle ScholarPubMed
Kass, MD, Rosenthal, MC, Pottackal, J, McGann JP. Fear learning enhances neural responses to threat-predictive sensory stimuli. Science. 2013;342(6164):13891392.CrossRefGoogle ScholarPubMed
Ahs, F, Miller, SS, Gordon, AR, Lundstrom JN. Aversive learning increases sensory detection sensitivity. Biol Psychology. 2013;92(2):135141.CrossRefGoogle ScholarPubMed
Hoenen, M, Wolf, OT, Pause, BM. The impact of stress on odor perception. Perception. 2017;46(3–4):366376.CrossRefGoogle ScholarPubMed
Krusemark, EA, Li, W. Enhanced olfactory sensory perception of threat in anxiety: an event-related fMRI study. Chemosens Percept. 2012;5(1):3745.CrossRefGoogle ScholarPubMed
La Buissonnière-Ariza, V, Lepore, F, Kojok, KM, Frasnelli J. Increased odor detection speed in highly anxious healthy adults. Chem Senses. 2013;38(7):577584.CrossRefGoogle ScholarPubMed
Pacharra, M, Schäper, M, Kleinbeck, S, Blaszkewicz M, van Thriel C. Olfactory acuity and automatic associations to odor words modulate adverse effects of ammonia. Chemosens Percept. 2016;9(1):2736.CrossRefGoogle Scholar
Jovanovic, H, Perski, A, Berglund, H, Savic I. Chronic stress is linked to 5-HT1A receptor changes and functional disintegration of the limbic networks. Neuroimage. 2011;55(3):11781188.CrossRefGoogle ScholarPubMed
Takahashi, T, Itoh, H, Nishikawa, Y, Higuchi Y, Nakamura M, Sasabayashi D, et al. Possible relation between olfaction and anxiety in healthy subjects. Psychiatry Clin Neurosci. 2015;69(7):431438.CrossRefGoogle ScholarPubMed
Berlin, HA, Stern, ER, Ng, J, Zhang S, Rosenthal D, Turetzky R, et al. Altered olfactory processing and increased insula activity in patients with obsessive-compulsive disorder: an fMRI study. Psychiatry Res Neuroimaging. 2017;262:1524.CrossRefGoogle Scholar
Burón, E, Bulbena, A, Bulbena-Cabré, A. Olfactory functioning in panic disorder. J Affect Disord. 2015;175:292298.CrossRefGoogle ScholarPubMed
Clepce, M, Reich, K, Gossler, A, Kornhuber J, Thuerauf N. Olfactory abnormalities in anxiety disorders. Neurosci Lett. 2012;511(1):4346.CrossRefGoogle ScholarPubMed
Cortese, BM, Schumann, AY, Howell, AN, McConnell PA, Yang QX, Uhde TW. Preliminary evidence for differential olfactory and trigeminal processing in combat veterans with and without PTSD. Neuroimage Clin. 2017;17:378387.CrossRefGoogle ScholarPubMed
Pause, BM, Adolph, D, Prehn-Kristensen, A, Ferstl R. Startle response potentiation to chemosensory anxiety signals in socially anxious individuals. Int J Psychophysiol. 2009;74(2):8892.CrossRefGoogle ScholarPubMed
Segalàs, C, Labad, J, Alonso, P, Real E, Subira M, Bueno B, et al. Olfactory identification and discrimination in obsessive-compulsive disorder. Depress Anxiety. 2011;28(10):932940.CrossRefGoogle ScholarPubMed
Cortese, BM, Leslie, K, Uhde, TW. Differential odor sensitivity in PTSD: implications for treatment and future research. J Affect Disord. 2015;179:2330.CrossRefGoogle ScholarPubMed
Kreutzer, R, Neutra, RR, Lashuay, N. Prevalence of people reporting sensitivities to chemicals in a population based survey. Am J Epidemiol. 1999;150(1):112.CrossRefGoogle Scholar
Meggs, WJ, Dunn, KA, Dunn, KA, Goodman PE, Davidoff AL. Prevalence and nature of allergy and chemical sensitivity in a general population. Arch Environ Health. 1996;51(4):275282.CrossRefGoogle Scholar
Bailer, J, Witthöft, M, Rist, F. The Chemical Odor Sensitivity Scale: reliability and validity of a screening instrument for idiopathic environmental intolerance. J Psychosom Res. 2006;61(1):7179.CrossRefGoogle ScholarPubMed
Cullen, MR. The worker with multiple chemical sensitivities: an overview. Occup Med. 1987;2(4):655661.Google ScholarPubMed
Miller, CA. Toxicant-induced loss of tolerance—an emerging theory of disease? Environ Health Perspect. 1997;105(2):445453.Google Scholar
Sparks, PJ, Daniell, W, Black, DW, Kipen HM, Altman LC, Simon GE, et al. Multiple chemical sensitivity syndrome: a clinical perspective. I. Case definition, theories of pathogenesis, and research needs. J Occup Med. 1994;36(7):718730.Google ScholarPubMed
Doty, RL, Deems, DA, Frye, RE, Pelberg R, Shapiro A. Olfactory sensitivity, nasal resistance, and autonomic function in patients with multiple chemical sensitivities. Arch Otolaryngol Head Neck Surg. 1988;114(12):14221427.CrossRefGoogle ScholarPubMed
Kärnekull, SC, Jönsson, FU, Larsson, M, Olofsson, JK. Affected by smells? Environmental chemical responsivity predicts odor perception. Chem Senses. 2011;36(7):641648.CrossRefGoogle ScholarPubMed
Bell, IR, Miller, CS, Schwartz, GE, Peterson JM, Amend D. Neuropsychiatric and somatic characteristics of young adults with and without self-reported chemical odor intolerance and chemical sensitivity. Arch Environ Health. 1996;51(1):921.CrossRefGoogle ScholarPubMed
Bell, IR, Peterson, JM, Schwartz, GE, Amend D. Self-reported illness from chemical odors in young adults without clinical syndromes or occupational exposures. Arch Environ Health. 1994;48(1):613.CrossRefGoogle Scholar
Devriese, S, Winters, W, Stegen, K, Van Diest I, Veulemans H, Nemery B, et al. Generalization of acquired somatic symptoms in response to odors: a Pavlovian perspective on multiple chemical sensitivity. Psychosom Med. 2000;62(6):751759.CrossRefGoogle ScholarPubMed
Doty, RL. The Snap & Sniff® Threshold Test Administration Manual. Haddon Heights, NJ: Sensonics, Inc.; 2015.Google Scholar
Taylor, S, Koch, WJ, McNally, RJ, Crockett DJ. Conceptualizations of anxiety sensitivity. Psychol Assess. 1992;4(2):245250.CrossRefGoogle Scholar
Osman, A, Gutierrez, PM, Smith, K, Fang Q, Lozano G, Devine A. The Anxiety Sensitivity Index-3: analyses of dimensions, reliability estimates, and correlates in nonclinical samples. J Pers Assess. 2010;92(1):4552.CrossRefGoogle ScholarPubMed
Allan, NP, Korte, KJ, Capron, DW, Raines AM, Schmidt NB. Factor mixture modeling of anxiety sensitivity: a three-class structure. Psychol Assess. 2014;26(4):11841195.CrossRefGoogle ScholarPubMed
Allan, NP, Raines, AM, Capron, DW, Norr AM, Zvolensky MJ, Schmidt NB. Identification of anxiety sensitivity classes and clinical cut-scores in a sample of adult smokers: results from a factor mixture model. J Anxiety Disord. 2014;28(7):696703.CrossRefGoogle Scholar
Spielberger, CD, Gorsuch, RL, Lushene, R, Vagg PR, Jacobs GA. Manual for the State-Trait Anxiety Inventory. Palo Alto, CA: Consulting Psychologists Press; 1983.Google Scholar
Kendall, PC, Finch, AJ, Auerbach, SM, Hooke JF, Mikulka PJ. The State-Trait Anxiety Inventory: a systematic evaluation. J Consul Clin Psychol. 1976;44(3):406412.CrossRefGoogle ScholarPubMed
Barnes, LLB, Harp, D, Jung, WS. Reliability generalization of scores on the Spielberger State-Trait Anxiety Inventory. Educational and Psychological Measurement. 2002;62(4):603618.CrossRefGoogle Scholar
Hishinuma, ES, Miyamoto, RH, Nishimura, ST, Goebert DA, Yuen NYC, Makini GK, et al. Prediction of anxiety disorders using the State-Trait Anxiety Inventory for multiethnic adolescents. J Anxiety Disord. 2001;15(6):511533.CrossRefGoogle ScholarPubMed
Kabakoff, RI, Segal, DL, Hersen, M, Van Hasselt VS. Psychometric properties and diagnostic utility of the Beck Anxiety Inventory and the state-trait anxiety inventory with older adult psychiatric inpatients. J Anxiety Disord. 1997;11(1):3347.CrossRefGoogle Scholar
Spielberger, CD. State-Trait Anxiety Inventory: Bibliography. 2nd ed. Palo Alto, CA: Consulting Psychologists Press; 1989.Google Scholar
Vautier, S. A longitudinal SEM model approach to STAI data: two comprehensive multitrait-multistate models. J Pers Assess. 2004;83(2):167179.CrossRefGoogle Scholar
Dennis, CL, Coghlan, M, Vigod, S. Can we identify mothers at-risk for postpartum anxiety in the immediate postpartum period using the State-Trait Anxiety Inventory? J Affect Disord. 2013;150(3):12171220.CrossRefGoogle ScholarPubMed
Fisher, PL, Durham, RC. Recovery rates in generalized anxiety disorder following psychological therapy: an analysis of clinically significant change in the STAI-T across outcome studies since 1990. Psychol Med. 1999;29(6):14251434.CrossRefGoogle ScholarPubMed
Holmes, TH, Rahe, RH. The social readjustment rating scale. J Psychosom Res. 1967;11(2):213218.CrossRefGoogle ScholarPubMed
Masuda, M, Holmes, TH. Magnitude estimations of social readjustments. J Psychosom Res. 1967;11(2):219225.CrossRefGoogle ScholarPubMed
Scully, JA, Tosi, H, Banning, K. Life Events Checklists: revisiting the Social Readjustment Rating Scale after 30 years. Educational and Psychological Measurement. 2000;60(6):864876.CrossRefGoogle Scholar
Gray, MJ, Litz, BT, Hsu, JL, et al. Psychometric properties of the Life Events Checklist. Assessment. 2004;11(4):330341.CrossRefGoogle ScholarPubMed
Meyer, TJ, Miller, ML, Metzger, RL, et al. Development and validation of the Penn State Worry Questionnaire. Behav Res Ther. 1990;28(6):487495.CrossRefGoogle ScholarPubMed
Brown, TA, Antony, MM, Barlow, DH. Psychometric properties of the Penn State Worry Questionnaire in a clinical anxiety disorders sample. Behav Res Ther. 1992;30(1):3337.CrossRefGoogle Scholar
Kroenke, K, Spitzer, RL. The PHQ-9: a new depression diagnostic and severity measure. Psychiatric Annals. 2002;32(9):509515.CrossRefGoogle Scholar
Manea, L, Gilbody, S, McMillan, D. Optimal cut-off score for diagnosing depression with the Patient Health Questionnaire (PHQ-9): a meta-analysis. CMAJ. 2012;184(3):191196.CrossRefGoogle ScholarPubMed
Martin, A, Rief, W, Klaiberg, A, et al. Validity of the brief Patient Health Questionnaire mood scale (PHQ-9) in the general population. Gen Hosp Psychiatry. 2006;28(1):7177.CrossRefGoogle Scholar
Buysse, DJ, Reynolds, CF, Monk, TH, et al. The Pittsburg Sleep Quality Index: a new instrument for psychiatric practice and research. Psychiatry Res. 1989;28(2):193213.CrossRefGoogle Scholar
Carpentera, JS, Andrykowskia, MA. Psychometric evaluation of the Pittsburg Sleep Quality Index. J Psychosom Res. 1998;45(1):513.CrossRefGoogle Scholar
Frenkel, TI, Lamy, D, Algom, D, et al. Individual differences in perceptual sensitivity and response bias in anxiety: evidence from emotional faces. Cognition and Emotion. 2009;23(4):688700.CrossRefGoogle Scholar
Gentili, C, Cristea, IA, Angstadt, M, et al. Beyond emotions: a meta-analysis of neural response within face processing system in social anxiety. Exp Biol Med. 2016;241(3):225237.CrossRefGoogle ScholarPubMed
Maltz, W. Treating the sexual intimacy concerns of sexual abuse survivors. Sexual and Relationship Therapy. 2002;17(4):321327.CrossRefGoogle Scholar
McNally, RJ. Is anxiety sensitivity distinguishable from trait anxiety? Reply to Lilienfeld, Jacob, and Turner (1989). J Abnorm Psychol. 1989;98(2):193194.CrossRefGoogle Scholar
LeDoux, J. Rethinking the emotional brain. Neuron. 2012;73(4):653676.CrossRefGoogle ScholarPubMed
Price, JL. Olfactory system. In: Paxinos G, ed. The Human Nervous System. San Diego, CA: Academic Press; 1990.Google Scholar
Etkin, A, Wager, TD. Functional neuroimaging of anxiety: a meta-analysis of emotional processing in PTSD, social anxiety disorder, and specific phobia. Am J Psychiatry. 2007;160(10):14761488.CrossRefGoogle Scholar
Chu, S, Downes, JJ. Proust nose best: odors are better cues of autobiographical memories. Mem Cogn. 2002;30(4):511518.CrossRefGoogle Scholar
Nickell, PV, Uhde, TW. Dose-response effects of intravenous caffeine in normal volunteers. Anxiety. 1994;1(4):161168.CrossRefGoogle ScholarPubMed
Daniels, JK, Vermetten, E. Odor-induced recall of emotional memories in PTSD—review and new paradigm for research. Exp Neurol. 2016;284(Pt B):168180.CrossRefGoogle ScholarPubMed
Doty, RL, Cometto-Muniz, JE. Trigeminal chemosensation. In: Doty RL, ed. Handbook of Olfaction and Gustation. 2nd ed. New York: Marcel Dekker; 2003:9811000.CrossRefGoogle Scholar
Doty, RL, Brugger, WE, Jurs, PC, et al. Intranasal trigeminal stimulation from odorous volatiles: psychometric responses from anosmic and normal humans. Physiol Behav. 1978;20(2):175185.CrossRefGoogle ScholarPubMed