Abstract
Structural neuroimaging studies on chronic smokers using voxel-based morphometry (VBM) had provided cumulative evidence of gray matter (GM) changes relative to nonsmokers. However, not all the studies reported entirely consistent findings. Here, we aimed at identifying consistent GM anomalies in chronic smokers by performing a meta-analysis, and a systematic search of VBM studies on chronic smokers and nonsmokers published in PubMed and Embase database from 2000 to April 2012. Meta-analysis was performed using a newly improved voxel-based meta-analytic tool, namely effect size signed differential mapping, to quantitatively explore the GM abnormalities between chronic smokers and nonsmokers. A total of 7 eligible VBM studies involving 213 chronic smokers and 205 nonsmokers met the inclusion criteria. A considerable regional GM volume decrease was detected in the anterior cingulate cortex (ACC) (BA 24) extending to BA32 in chronic smokers. The findings remain largely unchanged in the entire brain jackknife sensitivity analyses. The results of the present meta-analysis provide evidence of GM changes in ACC in chronic smokers which may be an important potential therapeutic neuro-target for nicotine dependence.
Similar content being viewed by others
References
Heishman SJ, Kleykamp BA, Singleton EG (2010) Meta-analysis of the acute effects of nicotine and smoking on human performance. Psychopharmacology 210(4):453–469. doi:10.1007/s00213-010-1848-1
Danaei G, Ding EL, Mozaffarian D, Taylor B, Rehm J, Murray CJ, Ezzati M (2009) The preventable causes of death in the United States: comparative risk assessment of dietary, lifestyle, and metabolic risk factors. PLoS Med 6(4):e1000058. doi:10.1371/journal.pmed.1000058
DeMarini DM (2004) Genotoxicity of tobacco smoke and tobacco smoke condensate: a review. Mutat Res 567(2–3):447–474. doi:10.1016/j.mrrev.2004.02.001
Ezzati M, Lopez AD (2000) Estimates of global mortality attributable to smoking in 2003. Lancet 362(9387):847–852. doi:10.1016/s0140-6736(03)14338-3
Laugesen M, Fowles J (2005) Scope for regulation of cigarette smoke toxicity according to brand differences in published toxicant emissions. N Z Med J 118(1213):U1401
Almeida OP, Garrido GJ, Lautenschlager NT, Hulse GK, Jamrozik K, Flicker L (2008) Smoking is associated with reduced cortical regional gray matter density in brain regions associated with incipient Alzheimer disease. Am J Geriatr Psychiatry 16(1):92–98. doi:10.1097/JGP.0b013e318157cad2
Ott A, Slooter AJ, Hofman A, van Harskamp F, Witteman JC, Van Broeckhoven C, van Duijn CM, Breteler MM (1998) Smoking and risk of dementia and Alzheimer’s disease in a population-based cohort study: the Rotterdam Study. Lancet 351(9119):1840–1843
Anstey KJ, von Sanden C, Salim A, O’Kearney R (2007) Smoking as a risk factor for dementia and cognitive decline: a meta-analysis of prospective studies. Am J Epidemiol 166(4):367–378. doi:10.1093/aje/kwm116
Tyas SL, White LR, Petrovitch H, Webster Ross G, Foley DJ, Heimovitz HK, Launer LJ (2003) Mid-life smoking and late-life dementia: the Honolulu-Asia Aging Study. Neurobiol Aging 24(4):589–596
Swan GE, Lessov-Schlaggar CN (2007) The effects of tobacco smoke and nicotine on cognition and the brain. Neuropsychol Rev 17(3):259–273. doi:10.1007/s11065-007-9035-9
Lecacheux M, Karila L, Aubin HJ, Dupont P, Benyamina A, Maman J, Lebert A, Reynaud M (2009) Cognitive modifications associated with tobacco smoking. Presse Med 38(9):1241–1252. doi:10.1016/j.lpm.2009.01.017
Dome P, Lazary J, Kalapos MP, Rihmer Z (2010) Smoking, nicotine and neuropsychiatric disorders. Neurosci Biobehav Rev 34(3):295–342. doi:10.1016/j.neubiorev.2009.07.013
Sharma A, Brody AL (2009) In vivo brain imaging of human exposure to nicotine and tobacco. Handb Exp Pharmacol 192:145–171. doi:10.1007/978-3-540-69248-5_6
Azizian A, Monterosso J, O’Neill J, London ED (2009) Magnetic resonance imaging studies of cigarette smoking. Handb Exp Pharmacol 192:113–143. doi:10.1007/978-3-540-69248-5_5
Ashburner J, Friston KJ (2000) Voxel-based morphometry–the methods. Neuroimage 11(6 Pt 1):805–821. doi:10.1006/nimg.2000.0582
Ashburner J, Friston KJ (2001) Why voxel-based morphometry should be used. Neuroimage 14(6):1238–1243. doi:10.1006/nimg.2001.0961
Brody AL, Mandelkern MA, Jarvik ME, Lee GS, Smith EC, Huang JC, Bota RG, Bartzokis G, London ED (2004) Differences between smokers and nonsmokers in regional gray matter volumes and densities. Biol Psychiatry 55(1):77–84
Liao Y, Tang J, Liu T, Chen X, Hao W (2010) Differences between smokers and non-smokers in regional gray matter volumes: a voxel-based morphometry study. Addict Biol. doi:10.1111/j.1369-1600.2010.00250.x
Zhang X, Salmeron BJ, Ross TJ, Geng X, Yang Y, Stein EA (2011) Factors underlying prefrontal and insula structural alterations in smokers. Neuroimage 54(1):42–48. doi:10.1016/j.neuroimage.2010.08.008
Yu R, Zhao L, Lu L (2011) Regional grey and white matter changes in heavy male smokers. PLoS One 6(11):e27440. doi:10.1371/journal.pone.0027440
Gallinat J, Meisenzahl E, Jacobsen LK, Kalus P, Bierbrauer J, Kienast T, Witthaus H, Leopold K, Seifert F, Schubert F, Staedtgen M (2006) Smoking and structural brain deficits: a volumetric MR investigation. Eur J Neurosci 24(6):1744–1750. doi:10.1111/j.1460-9568.2006.05050.x
Morales AM, Lee B, Hellemann G, O’Neill J, London ED (2012) Gray-matter volume in methamphetamine dependence: Cigarette smoking and changes with abstinence from methamphetamine. Drug Alcohol Depend. doi:10.1016/j.drugalcdep.2012.02.017
Radua J, Mataix-Cols D (2009) Voxel-wise meta-analysis of grey matter changes in obsessive-compulsive disorder. Br J Psychiatry 195(5):393–402. doi:10.1192/bjp.bp.108.055046
Bora E, Fornito A, Yucel M, Pantelis C (2010) Voxelwise meta-analysis of gray matter abnormalities in bipolar disorder. Biol Psychiatry 67(11):1097–1105. doi:10.1016/j.biopsych.2010.01.020
Via E, Radua J, Cardoner N, Happe F, Mataix-Cols D (2011) Meta-analysis of gray matter abnormalities in autism spectrum disorder: should Asperger disorder be subsumed under a broader umbrella of autistic spectrum disorder? Arch Gen Psychiatry 68(4):409–418. doi:10.1001/archgenpsychiatry.2011.27
Pan PL, Song W, Shang HF (2012) Voxel-wise meta-analysis of gray matter abnormalities in idiopathic Parkinson’s disease. Eur J Neurol 19(2):199–206. doi:10.1111/j.1468-1331.2011.03474.x
Radua J, Mataix-Cols D, Phillips ML, El-Hage W, Kronhaus DM, Cardoner N, Surguladze S (2011) A new meta-analytic method for neuroimaging studies that combines reported peak coordinates and statistical parametric maps. Eur Psychiatry. doi:10.1016/j.eurpsy.2011.04.001
Simms ML, Kemper TL, Timbie CM, Bauman ML, Blatt GJ (2009) The anterior cingulate cortex in autism: heterogeneity of qualitative and quantitative cytoarchitectonic features suggests possible subgroups. Acta Neuropathol 118(5):673–684. doi:10.1007/s00401-009-0568-2
Allman JM, Hakeem A, Erwin JM, Nimchinsky E, Hof P (2001) The anterior cingulate cortex. The evolution of an interface between emotion and cognition. Ann N Y Acad Sci 935:107–117
Bush G, Luu P, Posner MI (2000) Cognitive and emotional influences in anterior cingulate cortex. Trends Cogn Sci 4(6):215–222
Ernst M, Heishman SJ, Spurgeon L, London ED (2001) Smoking history and nicotine effects on cognitive performance. Neuropsychopharmacology 25(3):313–319. doi:10.1016/s0893-133x(01)00257-3
Razani J, Boone K, Lesser I, Weiss D (2004) Effects of cigarette smoking history on cognitive functioning in healthy older adults. Am J Geriatr Psychiatry 12(4):404–411. doi:10.1176/appi.ajgp.12.4.404
Richards M, Jarvis MJ, Thompson N, Wadsworth ME (2003) Cigarette smoking and cognitive decline in midlife: evidence from a prospective birth cohort study. Am J Public Health 93(6):994–998
Jacobsen LK, Krystal JH, Mencl WE, Westerveld M, Frost SJ, Pugh KR (2005) Effects of smoking and smoking abstinence on cognition in adolescent tobacco smokers. Biol Psychiatry 57(1):56–66. doi:10.1016/j.biopsych.2004.10.022
Hong LE, Gu H, Yang Y, Ross TJ, Salmeron BJ, Buchholz B, Thaker GK, Stein EA (2009) Association of nicotine addiction and nicotine’s actions with separate cingulate cortex functional circuits. Arch Gen Psychiatry 66(4):431–441. doi:10.1001/archgenpsychiatry.2009.2
Hudkins M, O’Neill J, Tobias MC, Bartzokis G, London ED (2012) Cigarette smoking and white matter microstructure. Psychopharmacology 221(2):285–295. doi:10.1007/s00213-011-2621-9
Li X, Hartwell KJ, Borckardt J, Prisciandaro JJ, Saladin ME, Morgan PS, Johnson KA, Lematty T, Brady KT, George MS (2012) Volitional reduction of anterior cingulate cortex activity produces decreased cue craving in smoking cessation: a preliminary real-time fMRI study. Addict Biol. doi:10.1111/j.1369-1600.2012.00449.x
Tang DW, Fellows LK, Small DM, Dagher A (2012) Food and drug cues activate similar brain regions: a meta-analysis of functional MRI studies. Physiol Behav 106(3):317–324. doi:10.1016/j.physbeh.2012.03.009
Acknowledgments
We thank all the authors of the included studies. We especially thank Dr. Joaquim Radua for his kind help and suggestings.
Conflict of interest
There is no actual or potential financial and other conflict of interest related to the submitted manuscript.
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Pan, P., Shi, H., Zhong, J. et al. Chronic smoking and brain gray matter changes: evidence from meta-analysis of voxel-based morphometry studies. Neurol Sci 34, 813–817 (2013). https://doi.org/10.1007/s10072-012-1256-x
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10072-012-1256-x