Hostname: page-component-8448b6f56d-cfpbc Total loading time: 0 Render date: 2024-04-16T08:38:02.167Z Has data issue: false hasContentIssue false

Psychotic reactions to daily life stress and dopamine function in people with severe hearing impairment

Published online by Cambridge University Press:  08 December 2014

M. J. Gevonden*
Affiliation:
Department of Psychiatry and Psychology, South Limburg Mental Health Research and Teaching Network, EURON, Maastricht University, Maastricht, The Netherlands Rivierduinen Institute for Mental Health Care, Leiden, The Netherlands Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
I. Myin-Germeys
Affiliation:
Department of Psychiatry and Psychology, South Limburg Mental Health Research and Teaching Network, EURON, Maastricht University, Maastricht, The Netherlands
W. van den Brink
Affiliation:
Department of Psychiatry, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
J. van Os
Affiliation:
Department of Psychiatry and Psychology, South Limburg Mental Health Research and Teaching Network, EURON, Maastricht University, Maastricht, The Netherlands King's College London, King's Health Partners, Department of Psychosis Studies, Institute of Psychiatry, London, UK
J. P. Selten
Affiliation:
Department of Psychiatry and Psychology, South Limburg Mental Health Research and Teaching Network, EURON, Maastricht University, Maastricht, The Netherlands Rivierduinen Institute for Mental Health Care, Leiden, The Netherlands
J. Booij
Affiliation:
Department of Nuclear Medicine, Academic Medical Center, University of Amsterdam, Amsterdam, The Netherlands
*
*Address for correspondence: M. J. Gevonden, M.Sc., Department of Nuclear Medicine, Academic Medical Center, PO Box 22660, 1100 DD, Amsterdam, The Netherlands. (Email: m.gevonden@maastrichtuniversity.nl)

Abstract

Background.

Minor stresses measured in daily life have repeatedly been associated with increased momentary psychotic experiences, both in individuals with psychotic disorders and in persons who are genetically at an increased risk for these disorders. Severe hearing impairment (SHI) is an environmental risk factor for psychotic disorder, possibly due to the experience of social exclusion. The aim of the current study is to investigate whether people with SHI exhibit higher levels of psychotic reactivity to social stressors in daily life than normal-hearing controls and whether this reactivity is associated with decreased baseline dopamine (DA) D2/3 receptor availability and/or elevated DA release following a dexamphetamine challenge.

Method.

We conducted an experience sampling study in 15 young adults with SHI and 19 matched normal-hearing controls who had previously participated in a single photon emission computed tomography study measuring DA D2/3 receptor availability and DA release in response to dexamphetamine.

Results.

The association between social stress and momentary psychotic experiences in daily life was stronger among SHI participants than among normal-hearing controls. Interactions between social stress and baseline striatal DA D2/3 receptor availability or DA release were not significant in multilevel models of momentary psychotic experiences including age, sex and tobacco use.

Conclusions.

While both elevated striatal DA release and elevated psychotic stress reactivity have been found in the same population defined by an environmental risk factor, SHI, their inter-relationship cannot be established. Further research is warranted to clarify the association between biological and psychological endophenotypes and psychosis risk.

Type
Original Articles
Copyright
Copyright © Cambridge University Press 2014 

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

Allan, S, Gilbert, P (1995). A social comparison scale: psychometric properties and relationship to psychopathology. Personality and Individual Differences 19, 293299.CrossRefGoogle Scholar
Booij, J, Korn, P, Linszen, DH, van Royen, EA (1997). Assessment of endogenous dopamine release by methylphenidate challenge using iodine-123 iodobenzamide single-photon emission tomography. European Journal of Nuclear Medicine and Molecular Imaging 24, 674677.CrossRefGoogle ScholarPubMed
Brunelin, J, d’ Amato, T, Brun, P, Bediou, B, Kallel, L, Senn, M, Poulet, E, Saoud, M (2007). Impaired verbal source monitoring in schizophrenia: an intermediate trait vulnerability marker? Schizophrenia Research 89, 287292.CrossRefGoogle ScholarPubMed
Brunelin, J, Fecteau, S, Suaud-Chagny, M-F (2013). Abnormal striatal dopamine transmission in schizophrenia. Current Medicinal Chemistry 20, 397404.Google ScholarPubMed
Collip, D, Myin-Germeys, I, Van Os, J (2008). Does the concept of “sensitization” provide a plausible mechanism for the putative link between the environment and schizophrenia? Schizophrenia Bulletin 34, 220.CrossRefGoogle ScholarPubMed
Cooper, AF (1976). Deafness and psychiatric illness. British Journal of Psychiatry 129, 216.CrossRefGoogle ScholarPubMed
David, A, Malmberg, A, Lewis, G, Brandt, L, Allebeck, P (1995). Are there neurological and sensory risk factors for schizophrenia? Schizophrenia Research 14, 247251.CrossRefGoogle ScholarPubMed
Delespaul, PA (1995). Assessing Schizophrenia in Daily Life. UPM, Universitaire Pers Maastricht: Maastricht.Google Scholar
Egerton, A, Chaddock, CA, Winton-Brown, TT, Bloomfield, MAP, Bhattacharyya, S, Allen, P, McGuire, PK, Howes, OD (2013). Presynaptic striatal dopamine dysfunction in people at ultra-high risk for psychosis: findings in a second cohort. Biological Psychiatry 74, 106112.CrossRefGoogle ScholarPubMed
Fehr, MD, Yakushev, MD, Hohmann, DP, Buchholz, MS, Landvogt, MD, Deckers, H, Eberhardt, A, Kläger, M, Smolka, MD, Scheurich, PD, Dielentheis, MD, Schmidt, MD, Rösch, PD, Bartenstein, MD, Gründer, MD, Schreckenberger, MD (2008). Association of low striatal dopamine D2 receptor availability with nicotine dependence similar to that seen with other drugs of abuse. American Journal of Psychiatry 165, 507514.CrossRefGoogle ScholarPubMed
Fellinger, J, Holzinger, D, Gerich, J, Goldberg, D (2007). Mental distress and quality of life in the hard of hearing. Acta Psychiatrica Scandinavica 115, 243245.CrossRefGoogle ScholarPubMed
Fors, A, Abel, KM, Wicks, S, Magnusson, C, Dalman, C (2013). Hearing and speech impairment at age 4 and risk of later non-affective psychosis. Psychological Medicine 43, 20672076.CrossRefGoogle ScholarPubMed
Garety, PA, Bebbington, P, Fowler, D, Freeman, D, Kuipers, E (2007). Implications for neurobiological research of cognitive models of psychosis: a theoretical paper. Psychological Medicine 37, 13771391.CrossRefGoogle ScholarPubMed
Garety, PA, Kuipers, E, Fowler, D, Freeman, D, Bebbington, PE (2001). A cognitive model of the positive symptoms of psychosis. Psychological Medicine 31, 189195.CrossRefGoogle ScholarPubMed
Gevonden, M, Booij, J, van den Brink, W, Heijtel, D, van Os, J, Selten, J (2014a). Increased release of dopamine in the striata of young adults with hearing impairment and its relevance for the social defeat hypothesis of schizophrenia. JAMA Psychiatry. Published online 01 10 2014 . doi:10.1001/jamapsychiatry.2014.1325.CrossRefGoogle ScholarPubMed
Gevonden, MJ, Selten, JP, Myin-Germeys, I, de Graaf, R, Ten Have, M, van Dorsselaer, S, van Os, J, Veling, W (2014 b). Sexual minority status and psychotic symptoms: findings from the Netherlands Mental Health Survey and Incidence Studies (NEMESIS). Psychological Medicine 44, 421434.CrossRefGoogle ScholarPubMed
Gilbert, P, Allan, S (1998). The role of defeat and entrapment (arrested flight) in depression: an exploration of an evolutionary view. Psychological Medicine 28, 585598.CrossRefGoogle ScholarPubMed
Goldstein, H (2005). Multilevel models. In Encyclopedia of Biostatistics (ed. Goldstein, H.). John Wiley & Sons, Ltd: Chichester. http://onlinelibrary.wiley.com/doi/10.1002/0470011815.b2a09031/abstract Google Scholar
Hasson, D, Theorell, T, Wallén, MB, Leineweber, C, Canlon, B (2011). Stress and prevalence of hearing problems in the Swedish working population. BMC Public Health 11, 130.CrossRefGoogle ScholarPubMed
Howes, OD, Montgomery, AJ, Asselin, M-C, Murray, RM, Valli, I, Tabraham, P, Bramon-Bosch, E, Valmaggia, L, Johns, L, Broome, M, McGuire, PK, Grasby, PM (2009). Elevated striatal dopamine function linked to prodromal signs of schizophrenia. Archives of General Psychiatry 66, 1320.CrossRefGoogle ScholarPubMed
Järvelin, MR, Mäki-Torkko, E, Sorri, MJ, Rantakallio, PT (1997). Effect of hearing impairment on educational outcomes and employment up to the age of 25 years in northern Finland. British Journal of Audiology 31, 165175.CrossRefGoogle Scholar
Keefe, RSE, Arnold, MC, Bayen, UJ, Harvey, PD (1999). Source monitoring deficits in patients with schizophrenia; a multinomial modelling analysis. Psychological Medicine 29, 903914.CrossRefGoogle ScholarPubMed
Kegeles, LS, Abi-Dargham, A, Frankle, WG, Gil, R, Cooper, TB, Slifstein, M, Hwang, D-R, Huang, Y, Haber, SN, Laruelle, M (2010). Increased synaptic dopamine function in associative regions of the striatum in schizophrenia. Archives of General Psychiatry 67, 231239.CrossRefGoogle ScholarPubMed
Lardinois, M, Lataster, T, Mengelers, R, Van Os, J, Myin-Germeys, I (2011). Childhood trauma and increased stress sensitivity in psychosis. Acta Psychiatrica Scandinavica 123, 2835.CrossRefGoogle ScholarPubMed
Laruelle, M, Abi-Dargham, A, Gil, R, Kegeles, L, Innis, R (1999). Increased dopamine transmission in schizophrenia: relationship to illness phases. Biological Psychiatry 46, 5672.CrossRefGoogle ScholarPubMed
Laruelle, M, Abi-Dargham, A, van Dyck, CH, Rosenblatt, W, Zea-Ponce, Y, Zoghbi, SS, Baldwin, RM, Charney, DS, Hoffer, PB, Kung, HF, Innis, RB (1995). SPECT imaging of striatal dopamine release after amphetamine challenge. Journal of Nuclear Medicine 36, 11821190.Google ScholarPubMed
Lataster, J, Collip, D, Ceccarini, J, Haas, D, Booij, L, van Os, J, Pruessner, J, Van Laere, K, Myin-Germeys, I (2011). Psychosocial stress is associated with in vivo dopamine release in human ventromedial prefrontal cortex: a positron emission tomography study using [18F]fallypride. NeuroImage 58, 10811089.CrossRefGoogle ScholarPubMed
Lataster, T, Valmaggia, L, Lardinois, M, van Os, J, Myin-Germeys, I (2013). Increased stress reactivity: a mechanism specifically associated with the positive symptoms of psychotic disorder. Psychological Medicine 43, 13891400.CrossRefGoogle ScholarPubMed
Martinez, D, Slifstein, M, Broft, A, Mawlawi, O, Hwang, D-R, Huang, Y, Cooper, T, Kegeles, L, Zarahn, E, Abi-Dargham, A, Haber, SN, Laruelle, M (2003). Imaging human mesolimbic dopamine transmission with positron emission tomography. Part II: amphetamine-induced dopamine release in the functional subdivisions of the striatum. Journal of Cerebral Blood Flow and Metabolism 23, 285300.CrossRefGoogle ScholarPubMed
Mathers, CD, Fat, DM, Boerma, J (2008). The Global Burden of Disease: 2004 Update. World Health Organization: Geneva.CrossRefGoogle Scholar
Mathers, CD, Loncar, D (2006). Projections of global mortality and burden of disease from 2002 to 2030. PLoS Medicine 3, e442.CrossRefGoogle ScholarPubMed
Mawlawi, O, Martinez, D, Slifstein, M, Broft, A, Chatterjee, R, Hwang, D-R, Huang, Y, Simpson, N, Ngo, K, Van Heertum, R, Laruelle, M (2001). Imaging human mesolimbic dopamine transmission with positron emission tomography: I. Accuracy and precision of D 2 receptor parameter measurements in ventral striatum. Journal of Cerebral Blood Flow and Metabolism 21, 10341057.CrossRefGoogle ScholarPubMed
Meyer, IH (2003). Prejudice, social stress, and mental health in lesbian, gay, and bisexual populations: conceptual issues and research evidence. Psychological Bulletin 129, 674697.CrossRefGoogle ScholarPubMed
Mizrahi, R, Addington, J, Rusjan, PM, Suridjan, I, Ng, A, Boileau, I, Pruessner, JC, Remington, G, Houle, S, Wilson, AA (2012). Increased stress-induced dopamine release in psychosis. Biological Psychiatry 71, 561567.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, Delespaul, P, Van Os, J (2005 a). Behavioural sensitization to daily life stress in psychosis. Psychological Medicine 35, 733741.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, Krabbendam, L, Delespaul, PA, Van Os, J (2003). Do life events have their effect on psychosis by influencing the emotional reactivity to daily life stress? Psychological Medicine 33, 327333.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, Marcelis, M, Krabbendam, L, Delespaul, P, van Os, J (2005 b). Subtle fluctuations in psychotic phenomena as functional states of abnormal dopamine reactivity in individuals at risk. Biological Psychiatry 58, 105110.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, Oorschot, M, Collip, D, Lataster, J, Delespaul, P, van Os, J (2009). Experience sampling research in psychopathology: opening the black box of daily life. Psychological Medicine 39, 15331547.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, van Os, J (2007). Stress-reactivity in psychosis: evidence for an affective pathway to psychosis. Clinical Psychology Review 27, 409424.CrossRefGoogle ScholarPubMed
Myin-Germeys, I, van Os, J, Schwartz, JE, Stone, AA, Delespaul, PA (2001). Emotional reactivity to daily life stress in psychosis. Archives of General Psychiatry 58, 11371144.CrossRefGoogle ScholarPubMed
Palmier-Claus, JE, Myin-Germeys, I, Barkus, E, Bentley, L, Udachina, A, Delespaul, PA, Lewis, SW, Dunn, G (2011). Experience sampling research in individuals with mental illness: reflections and guidance. Acta Psychiatrica Scandinavica 123, 1220.CrossRefGoogle ScholarPubMed
Pierre, PV, Fridberger, A, Wikman, A, Alexanderson, K (2012). Self-reported hearing difficulties, main income sources, and socio-economic status; a cross-sectional population-based study in Sweden. BMC Public Health 12, 874.CrossRefGoogle ScholarPubMed
Pohjalainen, T, Rinne, JO, Någren, K, Syvälahti, E, Hietala, J (1998). Sex differences in the striatal dopamine D2 receptor binding characteristics in vivo . American Journal of Psychiatry 155, 768773.Google ScholarPubMed
Pruessner, JC, Champagne, F, Meaney, MJ, Dagher, A (2004). Dopamine release in response to a psychological stress in humans and its relationship to early life maternal care: a positron emission tomography study using [11C]raclopride. Journal of Neuroscience 24, 28252831.CrossRefGoogle Scholar
Rinne, JO, Hietala, J, Ruotsalainen, U, Säkö, E, Laihinen, A, Någren, K, Lehikoinen, P, Oikonen, V, Syvälahti, E (1993). Decrease in human striatal dopamine D2 receptor density with age: a PET study with [11C]raclopride. Journal of Cerebral Blood Flow and Metabolism 13, 310314.CrossRefGoogle ScholarPubMed
Russell, DW (1996). UCLA Loneliness Scale (version 3): reliability, validity, and factor structure. Journal of Personality Assessment 66, 2040.CrossRefGoogle ScholarPubMed
Schmand, BA, Bakker, D, Saan, RJ, Louman, J (1991). De Nederlandse Leestest voor Volwassenen: een maat voor het premorbide intelligentieniveau (The Dutch Reading Test for Adults: a measure of premorbid intelligence level). Tijdschrift voor Gerontologie en Geriatrie 22, 1519.Google ScholarPubMed
Schwartz, JE, Stone, AA (1998). Strategies for analyzing ecological momentary assessment data. Health Psychology: Official Journal of the Division of Health Psychology, American Psychological Association 17, 616.CrossRefGoogle ScholarPubMed
Selten, J-P, Cantor-Graae, E (2007). Hypothesis: social defeat is a risk factor for schizophrenia? British Journal of Psychiatry 191, s9s12.CrossRefGoogle Scholar
Selten, JP, van der Ven, E, Rutten, BP, Cantor-Graae, E (2013). The social defeat hypothesis of schizophrenia: an update. Schizophrenia Bulletin 39, 11801186.CrossRefGoogle ScholarPubMed
Snijders, TAB, Bosker, RJ (1999). Multilevel Analysis: An Introduction to Basic and Advanced Multilevel Modeling, pp. 23, 341–342. Sage Publications: London.Google Scholar
Soliman, A, O'Driscoll, GA, Pruessner, J, Holahan, A-LV, Boileau, I, Gagnon, D, Dagher, A (2008). Stress-induced dopamine release in humans at risk of psychosis: a [ 11C]raclopride PET study. Neuropsychopharmacology 33, 20332041.CrossRefGoogle ScholarPubMed
Stam, M, Kostense, PJ, Festen, JM, Kramer, SE (2013). The relationship between hearing status and the participation in different categories of work: demographics. Work 46, 207219.CrossRefGoogle Scholar
Stefanis, N, Thewissen, V, Bakoula, C, van Os, J, Myin-Germeys, I (2006). Hearing impairment and psychosis: a replication in a cohort of young adults. Schizophrenia Research 85, 266272.CrossRefGoogle Scholar
Stevens, G, Flaxman, S, Brunskill, E, Mascarenhas, M, Mathers, CD, Finucane, M (2013). Global and regional hearing impairment prevalence: an analysis of 42 studies in 29 countries. European Journal of Public Health 23, 146152.CrossRefGoogle ScholarPubMed
Sweeting, H, West, P (2001). Being different: correlates of the experience of teasing and bullying at age 11. Research Papers in Education 16, 225246.CrossRefGoogle Scholar
Velthorst, E, Levine, SZ, Henquet, C, de Haan, L, van Os, J, Myin-Germeys, I, Reichenberg, A (2013). To cut a short test even shorter: Reliability and validity of a brief assessment of intellectual ability in Schizophrenia – a control-case family study. Cognitive Neuropsychiatry 18, 574593.CrossRefGoogle Scholar
Van der Werf, M, Thewissen, V, Dominguez, MD, Lieb, R, Wittchen, H, van Os, J (2011). Adolescent development of psychosis as an outcome of hearing impairment: a 10-year longitudinal study. Psychological Medicine 41, 477485.CrossRefGoogle ScholarPubMed
Van der Werf, M, van Boxtel, M, Verhey, F, Jolles, J, Thewissen, V, van Os, J (2007). Mild hearing impairment and psychotic experiences in a normal aging population. Schizophrenia Research 94, 180186.CrossRefGoogle Scholar