Smoking status as a potential confounder in the study of brain structure in schizophrenia

Journal of Psychiatric Research

Volumn 50, Issue 1, 2014, Pages 84-91

  Schneider, Claudia E ^a   White, Tonya ^b,c   Hass, Johanna ^a   Geisler, Daniel ^a   Wallace, Stuart R ^d,e   Roessner, Veit ^a   Holt, Daphne J ^d,e   Calhoun, Vince D ^f,g   Gollub, Randy L ^d,e   Ehrlich, Stefan ^a,d,e  

^a UNIVERSITY HOSPITAL CARL GUSTAV CARUS   (Germany)

^b ERASMUS MEDICAL CENTER   (Netherlands)

^c UNIVERSITY OF MINNESOTA MEDICAL SCHOOL   (United States)

^d MASSACHUSETTS GENERAL HOSPITAL   (United States)

^e MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^f University of New Mexico   (United States)

^g MIND RESEARCH NETWORK   (United States)

Author keywords

Brain volume; DLPFC; Hippocampus; MRI; Schizophrenia; Smoking

Indexed keywords

NEUROLEPTIC AGENT;

ADULT; ARTICLE; BRAIN REGION; BRAIN SIZE; COGNITION; CONFOUNDING VARIABLE; CONTROLLED STUDY; FEMALE; GRAY MATTER; HIPPOCAMPUS; HUMAN; MAJOR CLINICAL STUDY; MALE; NUCLEAR MAGNETIC RESONANCE IMAGING; PREFRONTAL CORTEX; PRIORITY JOURNAL; SCHIZOPHRENIA; SMOKING;

BRAIN VOLUME; DLPFC; HIPPOCAMPUS; MRI; SCHIZOPHRENIA; SMOKING;

ADULT; BRAIN; CEREBRAL CORTEX; CONFOUNDING FACTORS (EPIDEMIOLOGY); FEMALE; HIPPOCAMPUS; HUMANS; IMAGE PROCESSING, COMPUTER-ASSISTED; MAGNETIC RESONANCE IMAGING; MALE; NERVE FIBERS, UNMYELINATED; ORGAN SIZE; PREFRONTAL CORTEX; SCHIZOPHRENIA; SMOKING;

EID: 84892537819     PISSN: 00223956     EISSN: 18791379     Source Type: Journal    
DOI: 10.1016/j.jpsychires.2013.12.004     Document Type: Article

References (80)

1. Abnormal Involuntary Movement Scale (AIMS). Psychopharmacol Bull 1988, 24(4):781-783.
2. Addington D., Addington J., Maticka-Tyndale E. Assessing depression in schizophrenia: the Calgary Depression Scale. Br J Psychiatry Suppl December 1993, (22):39-44.
3. Adler L.E., Olincy A., Waldo M., Harris J.G., Griffith J., Stevens K. Schizophrenia, sensory gating, and nicotinic receptors. Schizophr Bull 1998, 24(2):189-202.
4. Adriano F., Caltagirone C., Spalletta G. Hippocampal volume reduction in first-episode and chronic schizophrenia: a review and meta-analysis. Neuroscientist April 2012, 18(2):180-200.
5. Andreasen N.C. Scale of assessment of negative symptoms (SANS) 1983, University of Iowa, Iowa city.
6. Andreasen N.C. Scale of the assessment of positive symptoms (SAPS) 1984, University of Iowa, Iowa city.
7. Andreasen N.C. Psychiatric symptoms you currently have-baseline (PSYCH-BASE) 1987, University of Iowa, Iowa city.
8. Andreasen N.C., Flaum M., Arndt S. The comprehensive assessment of symptoms and history (CASH). An instrument for assessing diagnosis and psychopathology. Arch Gen Psychiatry August 1992, 49(8):615-623.
9. Annett M. Aclassification of hand preference by association analysis. Br J Psychol August 1970, 61(3):303-321.
10. Barbey A.K., Koenigs M., Grafman J. Dorsolateral prefrontal contributions to human working memory. Cortex May 2013, 49(5):1195-1205.
11. Barnes T.R.E. The Barnes Akathisia rating Scale-revisited. JPsychopharmacol (Oxford) December 2003, 17(4):365-370.
12. Beatty W.W., Jocic Z., Monson N., Staton R.D. Memory and frontal lobe dysfunction in schizophrenia and schizoaffective disorder. JNerv Ment Dis July 1993, 181(7):448-453.
13. Becker T.M., Kerns J.G., Macdonald A.W., Carter C.S. Prefrontal dysfunction in first-degree relatives of schizophrenia patients during a Stroop task. Neuropsychopharmacology October 2008, 33(11):2619-2625.
14. Boyajian R.A., Otis S.M. Acute effects of smoking on human cerebral blood flow: a transcranial Doppler ultrasonography study. JNeuroimaging October 2000, 10(4):204-208.
15. Brody A.L., Mandelkern M.A., Jarvik M.E., Lee G.S., Smith E.C., Huang J.C. Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry January 2004, 55(1):77-84.
16. Buckner R.L., Head D., Parker J., Fotenos A.F., Marcus D., Morris J.C. Aunified approach for morphometric and functional data analysis in young, old, and demented adults using automated atlas-based head size normalization: reliability and validation against manual measurement of total intracranial volume. Neuroimage October 2004, 23(2):724-738.
17. Crespo-Facorro B., Barbadillo L., Pelayo-Terán J.M., Rodríguez-Sánchez J.M. Neuropsychological functioning and brain structure in schizophrenia. Int Rev Psychiatry August 2007, 19(4):325-336.
18. Cullen K.R., Wallace S., Magnotta V.A., Bockholt J., Ehrlich S., Gollub R.L., et al. Cigarette smoking and white matter microstructure in schizophrenia. Psychiatry Res February 2012, 201(2):152-158.
19. Davidson L.L., Heinrichs R.W. Quantification of frontal and temporal lobe brain-imaging findings in schizophrenia: a meta-analysis. Psychiatry Res February 2003, 122(2):69-87.
20. Desikan R.S., Ségonne F., Fischl B., Quinn B.T., Dickerson B.C., Blacker D., et al. An automated labeling system for subdividing the human cerebral cortex on MRI scans into gyral based regions of interest. Neuroimage July 2006, 31(3):968-980.
21. Durazzo T.C., Meyerhoff D.J., Nixon S.J. Interactive effects of chronic cigarette smoking and age on hippocampal volumes. Drug Alcohol Depend December 2013, 133(2):704-711.
22. Durazzo T.C., Meyerhoff D.J., Nixon S.J. Chronic cigarette smoking: implications for neurocognition and brain neurobiology. Int J Environ Res Public Health October 2010, 7(10):3760-3791.
23. Ehrlich S., Walton E., Roffman J.L., Weiss D., Puls I., Doehler N., et al. Smoking, but not malnutrition, influences promoter-specific DNA methylation of the proopiomelanocortin gene in patients with and without anorexia nervosa. Can J Psychiatry March 2012, 57(3):168-176.
24. Ehrlich S., Brauns S., Yendiki A., Ho B.-C., Calhoun V., Schulz S.C., et al. Associations of cortical thickness and cognition in patients with schizophrenia and healthy controls. Schizophr Bull 2012, 38(5):1050-1062.
25. Ehrlich S., Morrow E.M., Roffman J.L., Wallace S.R., Naylor M., Bockholt H.J., et al. The COMT Val108/158Met polymorphism and medial temporal lobe volumetry in patients with schizophrenia and healthy adults. Neuroimage November 2010, 53(3):992-1000.
26. First M.B., Spitzer R.L., Gibbon M., Williams J.B.W. Structured clinical interview for DSM-IV-TR Axis I disorders 2002, Biometrics Research, New York State Psychiatric Institute, New York.
27. Fischl B., Dale A.M. Measuring the thickness of the human cerebral cortex from magnetic resonance images. Proc Natl Acad Sci U S A September 2000, 97(20):11050-11055.
28. Fischl B., Salat D.H., Busa E., Albert M., Dieterich M., Haselgrove C., et al. Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron January 2002, 33(3):341-355.
29. Fischl B., Sereno M.I., Tootell R.B., Dale A.M. High-resolution intersubject averaging and a coordinate system for the cortical surface. Hum Brain Mapp 1999, 8(4):272-284.
30. Friedman L., Turner J.A., Stern H., Mathalon D.H., Trondsen L.C., Potkin S.G. Chronic smoking and the BOLD response to a visual activation task and a breath hold task in patients with schizophrenia and healthy controls. Neuroimage April 2008, 40(3):1181-1194.
31. Gallinat J., Lang U.E., Jacobsen L.K., Bajbouj M., Kalus P., von Haebler D., et al. Abnormal hippocampal neurochemistry in smokers: evidence from proton magnetic resonance spectroscopy at 3 T. JClin Psychopharmacol February 2007, 27(1):80-84.
32. Gallinat J., Meisenzahl E., Jacobsen L.K., Kalus P., Bierbrauer J., Kienast T., et al. Smoking and structural brain deficits: a volumetric MR investigation. Eur J Neurosci September 2006, 24(6):1744-1750.
33. Goldman A.L., Pezawas L., Mattay V.S., Fischl B., Verchinski B.A., Chen Q., et al. Widespread reductions of cortical thickness in schizophrenia and spectrum disorders and evidence of heritability. Arch Gen Psychiatry May 2009, 66(5):467-477.
34. Gur R.E., Cowell P.E., Latshaw A., Turetsky B.I., Grossman R.I., Arnold S.E., et al. Reduced dorsal and orbital prefrontal gray matter volumes in schizophrenia. Arch Gen Psychiatry August 2000, 57(8):761-768.
35. Haijma S.V., Van Haren N., Cahn W., Koolschijn P.C.M.P., Hulshoff Pol H.E., Kahn R.S. Brain volumes in schizophrenia: a meta-analysis in over 18,000 subjects. Schizophr Bull 2013, 39(5):1129-1138.
36. Van Haren N.E.M., Koolschijn P.C.M.P., Cahn W., Schnack H.G., Hulshoff Pol H.E., Kahn R.S. Cigarette smoking and progressive brain volume loss in schizophrenia. Eur Neuropsychopharmacol July 2010, 20(7):454-458.
37. Heatherton T.F., Kozlowski L.T., Frecker R.C., Fagerström K.O. The Fagerström test for nicotine dependence: a revision of the Fagerström tolerance questionnaire. Br J Addict September 1991, 86(9):1119-1127.
38. Heckers S. Neuroimaging studies of the hippocampus in schizophrenia. Hippocampus 2001, 11(5):520-528.
39. Heckers S., Konradi C. Hippocampal pathology in schizophrenia. Curr Top Behav Neurosci 2010, 4:529-553.
40. Hollingshead A. Two factor index of social position 1965, Yale University, New Haven.
41. Honea R., Crow T.J., Passingham D., Mackay C.E. Regional deficits in brain volume in schizophrenia: a meta-analysis of voxel-based morphometry studies. Am J Psychiatry December 2005, 162(12):2233-2245.
42. Jovicich J., Czanner S., Greve D., Haley E., van der Kouwe A., Gollub R., et al. Reliability in multi-site structural MRI studies: effects of gradient non-linearity correction on phantom and human data. Neuroimage April 2006, 30(2):436-443.
43. Jovicich J., Czanner S., Han X., Salat D., van der Kouwe A., Quinn B., et al. MRI-derived measurements of human subcortical, ventricular and intracranial brain volumes: reliability effects of scan sessions, acquisition sequences, data analyses, scanner upgrade, scanner vendors and field strengths. Neuroimage May 2009, 46(1):177-192.
44. Kikinis Z., Fallon J.H., Niznikiewicz M., Nestor P., Davidson C., Bobrow L., et al. Gray matter volume reduction in rostral middle frontal gyrus in patients with chronic schizophrenia. Schizophr Res November 2010, 123(2-3):153-159.
45. Kühn S., Schubert F., Gallinat J. Reduced thickness of medial orbitofrontal cortex in smokers. Biol Psychiatry December 2010, 68(11):1061-1065.
46. Kuperberg G.R., Broome M.R., McGuire P.K., David A.S., Eddy M., Ozawa F., et al. Regionally localized thinning of the cerebral cortex in schizophrenia. Arch Gen Psychiatry September 2003, 60(9):878-888.
47. De Leon J., Diaz F.J. Ameta-analysis of worldwide studies demonstrates an association between schizophrenia and tobacco smoking behaviors. Schizophr Res July 2005, 76(2-3):135-157.
48. Leyba L., Mayer A.R., Gollub R.L., Andreasen N.C., Clark V.P. Smoking status as a potential confound in the BOLD response of patients with schizophrenia. Schizophr Res September 2008, 104(1-3):79-84.
49. Liao Y., Tang J., Liu T., Chen X., Hao W. Differences between smokers and non-smokers in regional gray matter volumes: a voxel-based morphometry study. Addict Biol November 2012, 17(6):977-980.
50. Lopez-Garcia P., Aizenstein H.J., Snitz B.E., Walter R.P., Carter C.S. Automated ROI-based brain parcellation analysis of frontal and temporal brain volumes in schizophrenia. Psychiatry Res October 2006, 147(2-3):153-161.
51. Lucas C., Martin J. Smoking and drug interactions November 2013, http://www.australianprescriber.com/magazine/36/3/102/4.
52. Maher B.A., Manschreck T.C., Woods B.T., Yurgelun-Todd D.A., Tsuang M.T. Frontal brain volume and context effects in short-term recall in schizophrenia. Biol Psychiatry February 1995, 37(3):144-150.
53. Narr K.L., Toga A.W., Szeszko P., Thompson P.M., Woods R.P., Robinson D., et al. Cortical thinning in cingulate and occipital cortices in first episode schizophrenia. Biol Psychiatry July 2005, 58(1):32-40.
54. Nelson M.D., Saykin A.J., Flashman L.A., Riordan H.J. Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch Gen Psychiatry May 1998, 55(5):433-440.
55. Niemann K., Hammers A., Coenen V.A., Thron A., Klosterkötter J. Evidence of a smaller left hippocampus and left temporal horn in both patients with first episode schizophrenia and normal control subjects. Psychiatry Res August 2000, 99(2):93-110.
56. Parent A., Carpenter M. Human neuroanatomy 1995, Williams & Wilkins., Baltimore: MD.
57. Potkin S., Turner J., Fallon J., Lakatos A., Keator D., Guffanti G., et al. Gene discovery through imaging genetics: identification of two novel genes associated with schizophrenia. Mol Psychiatry 2009, 14(4):416-428.
58. Potkin S.G., Turner J.A., Brown G.G., McCarthy G., Greve D.N., Glover G.H., et al. Working memory and DLPFC inefficiency in schizophrenia: the FBIRN study. Schizophr Bull 2009, 35(1):19-31.
59. Rajkowska G., Goldman-Rakic P.S. Cytoarchitectonic definition of prefrontal areas in the normal human cortex: II. Variability in locations of areas 9 and 46 and relationship to the Talairach coordinate system. Cereb Cortex August 1995, 5(4):323-337.
60. Sanfilipo M., Lafargue T., Rusinek H., Arena L., Loneragan C., Lautin A., et al. Volumetric measure of the frontal and temporal lobe regions in schizophrenia: relationship to negative symptoms. Arch Gen Psychiatry May 2000, 57(5):471-480.
61. Saykin A.J., Gur R.C., Gur R.E., Mozley P.D., Mozley L.H., Resnick S.M., et al. Neuropsychological function in schizophrenia. Selective impairment in memory and learning. Arch Gen Psychiatry July 1991, 48(7):618-624.
62. Saykin A.J., Shtasel D.L., Gur R.E., Kester D.B., Mozley L.H., Stafiniak P., et al. Neuropsychological deficits in neuroleptic naive patients with first-episode schizophrenia. Arch Gen Psychiatry February 1994, 51(2):124-131.
63. Schultz C.C., Koch K., Wagner G., Roebel M., Nenadic I., Schachtzabel C., et al. Complex pattern of cortical thinning in schizophrenia: results from an automated surface based analysis of cortical thickness. Psychiatry Res May 2010, 182(2):134-140.
64. Segall J.M., Turner J.A., van Erp T.G.M., White T., Bockholt H.J., Gollub R.L., et al. Voxel-based morphometric multisite collaborative study on schizophrenia. Schizophr Bull January 2009, 35(1):82-95.
65. Seidman L.J., Pantelis C., Keshavan M.S., Faraone S.V., Goldstein J.M., Horton N.J., et al. Areview and new report of medial temporal lobe dysfunction as a vulnerability indicator for schizophrenia: a magnetic resonance imaging morphometric family study of the parahippocampal gyrus. Schizophr Bull 2003, 29(4):803-830.
66. Shenton M.E., Dickey C.C., Frumin M., McCarley R.W. Areview of MRI findings in schizophrenia. Schizophr Res April 2001, 49(1-2):1-52.
67. Shepherd A.M., Laurens K.R., Matheson S.L., Carr V.J., Green M.J. Systematic meta-review and quality assessment of the structural brain alterations in schizophrenia. Neurosci Biobehav Rev April 2012, 36(4):1342-1356.
68. Squire L.R., Zola-Morgan S. The medial temporal lobe memory system. Science September 1991, 253(5026):1380-1386.
69. Stonnington C.M., Tan G., Klöppel S., Chu C., Draganski B., Jack C.R., et al. Interpreting scan data acquired from multiple scanners: a study with Alzheimer's disease. Neuroimage February 2008, 39(3):1180-1185.
70. Takayanagi Y., Takahashi T., Orikabe L., Mozue Y., Kawasaki Y., Nakamura K., et al. Classification of first-episode schizophrenia patients and healthy subjects by automated MRI measures of regional brain volume and cortical thickness. PLoS ONE 2011, 6(6):e21047.
71. Tregellas J.R., Shatti S., Tanabe J.L., Martin L.F., Gibson L., Wylie K., et al. Gray matter volume differences and the effects of smoking on gray matter in schizophrenia. Schizophr Res December 2007, 97(1-3):242-249.
72. Voineskos A.N., Foussias G., Lerch J., Felsky D., Remington G., Rajji T.K., et al. Neuroimaging evidence for the deficit subtype of schizophrenia. JAMA Psychiatry May 2013, 70(5):472-480.
73. Watson D.R., Bai F., Barrett S.L., Turkington A., Rushe T.M., Mulholland C.C., et al. Structural changes in the hippocampus and amygdala at first episode of psychosis. Brain Imaging Behav March 2012, 6(1):49-60.
74. Weiss A.P., Heckers S. Neuroimaging of declarative memory in schizophrenia. Scand J Psychol July 2001, 42(3):239-250.
75. Wilkinson D. Wide Range achievement test 1993, Wide Range, Inc, Wilmington. 3rd ed.
76. Winterer G. Why do patients with schizophrenia smoke?. Curr Opin Psychiatry March 2010, 23(2):112-119.
77. Woods S.W. Chlorpromazine equivalent doses for the newer atypical antipsychotics. JClin Psychiatry June 2003, 64(6):663-667.
78. Wright I.C., Rabe-Hesketh S., Woodruff P.W., David A.S., Murray R.M., Bullmore E.T. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry January 2000, 157(1):16-25.
79. Ziedonis D., Hitsman B., Beckham J.C., Zvolensky M., Adler L.E., Audrain-McGovern J., et al. Tobacco use and cessation in psychiatric disorders: National Institute of Mental Health report. Nicotine Tob Res December 2008, 10(12):1691-1715.
80. Zilles D., Burke S., Schneider-Axmann T., Falkai P., Gruber O. Diagnosis-specific effect of familial loading on verbal working memory in schizophrenia. Eur Arch Psychiatry Clin Neurosci September 2009, 259(6):309-315.