Cigarette smoking and white matter microstructure
Open accessAbstract
Rationale Diffusion tensor imaging has been used before in testing associations between cigarette smoking and white matter integrity, with inconsistent results. Published reports indicate higher fractional anisotropy (FA, a measure of linear water diffusion) in some brain regions and lower FA in others in adult smokers compared to nonsmokers. Adolescent smokers exhibited elevated FA at several brain regions and a positive correlation of FA in the genu corpus callosum with exposure to smoking (pack-years).Objective To help resolve prior discrepancies, we studied adults, sampling multiple brain regions, and testing for relationships to clinical features of nicotine dependence and exposure to smoking.Methods Brain MRI scans (1.5 T) were acquired, and FA and apparent diffusion coefficient (ADC, a measure of random diffusion) were assayed in corpus callosum and prefrontal white matter, corona radiata, internal capsule, cingulum bundle, and hippocampal perforant fibers in 18 smokers (33.7 ± 7.9 years of age) and 18 age- and gender-matched nonsmokers.Results ADC showed no group difference, but smokers had higher (4.3-21.1%) FA than nonsmokers. The differences were significant in right prefrontal white matter, cingulum, and genu corpus callosum. FA in several regions was negatively correlated with nicotine dependence or cigarettes/day.Conclusions Combined with earlier findings, these results suggest a model of changing trajectories whereby FA is higher with tobacco exposure during adolescence and declines with continued smoking in adulthood. This notion is supported by the observation that, at multiple sampling sites, participants who had started smoking earlier in life had higher FA than those who had started later.
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Higher FA is more commonly observed in younger nicotine users.
“with higher FA more commonly observed in younger nicotine users (Hudkins et al., 2012; Jacobsen et al., 2007).”
From Substance abuse and white matter: Findings, limitations, and future of diffusion tensor imaging research (2019) · cites this paper as Hudkins et al., 2012
Regular nicotine use is associated with higher FA.
“and higher FA (Hudkins, O’Neill, Tobias, Bartzokis, & London, 2012; Wang et al., 2017).”
From Substance abuse and white matter: Findings, limitations, and future of diffusion tensor imaging research (2019) · cites this paper as Hudkins, O’Neill, Tobias, Bartzokis, & London, 2012
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Cites
The assessment and analysis of handedness: The Edinburgh inventory
Oldfield, R. C. (1971) · Neuropsychologia · doi:10.1016/0028-3932(71)90067-4 · Cited by 35,900 · see citing works
Advances in functional and structural MR image analysis and implementation as FSL
Smith, S. M., Jenkinson, M., Woolrich, M. W., Beckmann, C. F., Behrens, T. E. J., Johansen-Berg, H., Bannister, P. R., De Luca, M., Drobnjak, I., Flitney, D. E., et al. (2004) · NeuroImage · doi:10.1016/j.neuroimage.2004.07.051 · Cited by 13,630 · see citing works
The Fagerstrom Test for Nicotine Dependence: a revision of the Fagerstrom Tolerance Questionnaire
HEATHERTON, T. F., KOZLOWSKI, L. T., FRECKER, R. C., & FAGERSTROM, K. (1991) · British Journal of Addiction · doi:10.1111/j.1360-0443.1991.tb01879.x · Cited by 10,738 · see citing works
A global optimisation method for robust affine registration of brain images
Jenkinson, M., & Smith, S. M. (2001) · Medical Image Analysis · doi:10.1016/s1361-8415(01)00036-6 · Cited by 6,806 · see citing works
The basis of anisotropic water diffusion in the nervous system—A technical review.
Beaulieu, C. (2002) · NMR in Biomedicine · doi:10.1002/nbm.782 · Cited by 4,653 · see citing works
An Improved Diagnostic Evaluation Instrument for Substance Abuse Patients
McLellan, A. T., Luborsky, L. B., WOODY, G. E., & Brien, C. P. O. (1980) · The Journal of Nervous and Mental Disease · doi:10.1097/00005053-198001000-00006 · Cited by 3,163 · see citing works
Characterization and propagation of uncertainty in diffusion-weighted MR imaging
Behrens, T. E. J., Woolrich, M. W., Jenkinson, M., Johansen‐Berg, H., Nunes, R. G., Clare, S., Matthews, P. M., Brady, J. M., & Smith, S. M. (2003) · Magnetic Resonance in Medicine · doi:10.1002/mrm.10609 · Cited by 3,038 · see citing works
Danaei, G., Ding, E. L., Mozaffarian, D., Taylor, B., Rehm, J., Murray, C. J. L., & Ezzati, M. (2009) · PLoS Medicine · doi:10.1371/journal.pmed.1000058 · Cited by 2,860 · see citing works
(2009) · Elsevier eBooks · doi:10.1016/c2009-1-03742-3 · Cited by 1,332 · see citing works
The dynamic effects of nicotine on the developing brain
Dwyer, J. B., McQuown, S. C., & Leslie, F. M. (2009) · Pharmacology & Therapeutics · doi:10.1016/j.pharmthera.2009.02.003 · Cited by 559 · see citing works
White matter changes in mild cognitive impairment and AD: a diffusion tensor imaging study
Medina, D., deToledo-Morrell, L., Urresta, F., Gabrieli, J. D. E., Moseley, M., Fleischman, D., Bennett, D. A., Leurgans, S., Turner, D. A., & Stebbins, G. T. (2006) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2005.03.026 · Cited by 492 · see citing works
Cerebral White Matter Integrity and Cognitive Aging: Contributions from Diffusion Tensor Imaging
Madden, D. J., Bennett, I. J., & Song, A. W. (2009) · Neuropsychology Review · doi:10.1007/s11065-009-9113-2 · Cited by 463 · see citing works
Myelination of Cortical-hippocampal Relays During Late Adolescence
Benes, F. M. (1989) · Schizophrenia Bulletin · doi:10.1093/schbul/15.4.585 · Cited by 448 · see citing works
Due, D. L., Huettel, S. A., HALL, W. G., & Rubin, D. C. (2002) · American Journal of Psychiatry · doi:10.1176/appi.ajp.159.6.954 · Cited by 429 · see citing works
Bürgel, U., Amunts, K., Hömke, L., Mohlberg, H., Gilsbach, J. M., & Zilles, K. (2005) · NeuroImage · doi:10.1016/j.neuroimage.2005.08.040 · Cited by 425 · see citing works
Differences between smokers and nonsmokers in regional gray matter volumes and densities
Brody, A. L., Mandelkern, M. A., Jarvik, M. E., Lee, G. S., Smith, E. C., Huang, J. C.-S., Bota, R. G., Bartzokis, G., & London, E. D. (2003) · Biological Psychiatry · doi:10.1016/s0006-3223(03)00610-3 · Cited by 384 · see citing works
Self-citationThe perforant path: projections from the entorhinal cortex to the dentate gyrus
Witter, M. P. (2007) · Progress in brain research · doi:10.1016/s0079-6123(07)63003-9 · Cited by 358 · see citing works
Cognitive aging, executive function, and fractional anisotropy: a diffusion tensor MR imaging study.
Grieve, S. M., Williams, L. M., Paul, R. H., Clark, C. R., & Gordon, E. (2007) · PubMed Central · Cited by 350 · see citing works
Smoking and structural brain deficits: a volumetric MR investigation
Gallinat, J., Meisenzahl, E., Jacobsen, L. K., Kalus, P., Bierbrauer, J., Kienast, T., Witthaus, H., Leopold, K., Seifert, F., Schubert, F., et al. (2006) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2006.05050.x · Cited by 330 · see citing works
Hsu, J., Leemans, A., Bai, C., Lee, C.-H., Tsai, Y., Chiu, H., & Chen, W.-H. (2007) · NeuroImage · doi:10.1016/j.neuroimage.2007.09.017 · Cited by 313 · see citing works
Hoeft, F., Barnea‐Goraly, N., Haas, B. W., Golarai, G., Ng, D., Mills, D. L., Korenberg, J. R., Bellugi, U., Galaburda, A. M., & Reiss, A. L. (2007) · Journal of Neuroscience · doi:10.1523/jneurosci.3591-07.2007 · Cited by 305 · see citing works
Age‐Related Changes in Prefrontal White Matter Measured by Diffusion Tensor Imaging
SALAT, D. H., TUCH, D. S., HEVELONE, N. D., FISCHL, B., CORKIN, S., ROSAS, H. D., & DALE, A. M. (2005) · Annals of the New York Academy of Sciences · doi:10.1196/annals.1340.009 · Cited by 292 · see citing works
Ringman, J. M., O'Neill, J., Geschwind, D., Medina, L., Apostolova, L. G., Rodriguez, Y., Schaffer, B., Varpetian, A., Tseng, B., Ortiz, F., et al. (2007) · Brain · doi:10.1093/brain/awm102 · Cited by 290 · see citing works
Self-citationFactors underlying prefrontal and insula structural alterations in smokers
Zhang, X., Salmeron, B. J., Ross, T. J., Geng, X., Yang, Y., & Stein, E. A. (2011) · NeuroImage · doi:10.1016/j.neuroimage.2010.08.008 · Cited by 188 · see citing works
Gazdzinski, S., Durazzo, T. C., Studholme, C., Song, E., Banys, P., & Meyerhoff, D. J. (2005) · Alcoholism: Clinical & Experimental Research · doi:10.1097/01.alc.0000175018.72488.61 · Cited by 160 · see citing works
Almeida, O. P., Garrido, G. J., Lautenschlager, N. T., Hulse, G. K., Jamrozik, K. D., & Flicker, L. A. (2007) · American Journal of Geriatric Psychiatry · doi:10.1097/jgp.0b013e318157cad2 · Cited by 149 · see citing works
Jacobsen, L. K., Picciotto, M. R., Heath, C. J., Frost, S. J., Tsou, K. A., Dwan, R. A., Jackowski, M. P., Constable, R. T., & Mencl, W. E. (2007) · The Journal of Neuroscience · doi:10.1523/jneurosci.2402-07.2007 · Cited by 147 · see citing works
Reduced Thickness of Medial Orbitofrontal Cortex in Smokers
Kühn, S., Schubert, F., & Gallinat, J. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.08.004 · Cited by 137 · see citing works
Paul, R., Grieve, S., Niaura, R., David, S., Laidlaw, D., Cohen, R., Sweet, L., Taylor, G., Clark, R., Pogun, S., et al. (2008) · Nicotine & Tobacco Research · doi:10.1080/14622200701767829 · Cited by 129 · see citing works
Estimating WAIS IQ from the shipley institute of living scale using continuously adjusted age norms
Zachary, R. A., Paulson, M. J., & Gorsuch, R. L. (1985) · Journal of Clinical Psychology · doi:10.1002/1097-4679(198511)41:6 · Cited by 125 · see citing works
Regional Cerebral Blood Flow Responses to Smoking in Tobacco Smokers After Overnight Abstinence
Zubieta, J., Heitzeg, M. M., Xu, Y., Koeppe, R. A., Ni, L., Guthrie, S. K., & Domino, E. F. (2005) · American Journal of Psychiatry · doi:10.1176/appi.ajp.162.3.567 · Cited by 121 · see citing works
Decreased frontal white-matter integrity in abstinent methamphetamine abusers
Chung, A., Lyoo, I. K., Kim, S. J., Hwang, J., Bae, S. C., Sung, Y. H., Sim, M., Song, I. C., Kim, J. H., Chang, K. H., et al. (2006) · The International Journal of Neuropsychopharmacology · doi:10.1017/s1461145706007395 · Cited by 119 · see citing works
Kimes, A. S., Horti, A. G., London, E. D., Chefer, S. I., Contoreggi, C. S., Monique Ernst, D., Friello, P. J., Koren, A. O., Kurian, V., Matochik, J. A., et al. (2003) · The FASEB Journal · doi:10.1096/fj.02-0492fje · Cited by 113 · see citing works
Self-citationRegional cerebral blood flow and plasma nicotine after smoking tobacco cigarettes
Domino, E. F. (2003) · Progress in Neuro-Psychopharmacology and Biological Psychiatry · doi:10.1016/j.pnpbp.2003.10.011 · Cited by 95 · see citing works
Neuronal nicotinic acetylcholine receptor expression by O2A/oligodendrocyte progenitor cells
Rogers, S. W., Gregori, N. Z., Carlson, N. G., Gahring, L. C., & Noble, M. (2001) · Glia · doi:10.1002/1098-1136(20010315)33:4 · Cited by 94 · see citing works
White Matter Microstructure in Relation to Education in Aging and Alzheimer's Disease1
Teipel, S. J., Meindl, T., Wagner, M., Kohl, T., Bürger, K., Reiser, M. F., Herpertz, S. C., Möller, H., & Hampel, H. J. (2009) · Journal of Alzheimer s Disease · doi:10.3233/jad-2009-1077 · Cited by 92 · see citing works
White-matter abnormalities in brain during early abstinence from methamphetamine abuse
Tobias, M. C., O’Neill, J., Hudkins, M. R., Bartzokis, G., Dean, A. C., & London, E. D. (2010) · Psychopharmacology · doi:10.1007/s00213-009-1761-7 · Cited by 92 · see citing works
Self-citationBartzokis, G., Lu, P. H., Stewart, S. B., Oluwadara, B., Lucas, A. J., Pantages, J., Pratt, E., Sherin, J. E., Altshuler, L. L., Mintz, J., et al. (2009) · Schizophrenia Research · doi:10.1016/j.schres.2009.06.014 · Cited by 91 · see citing works
Self-citationDing, Y., Fowler, J. S., Logan, J., Wang, G., Telang, F., Garza, V., Biegon, A. R., Pareto, D., Rooney, W. D., Shea, C. E., et al. (2004) · Synapse · doi:10.1002/syn.20051 · Cited by 89 · see citing works
Lower diffusion in white matter of children with prenatal methamphetamine exposure
Cloak, C. C., Ernst, T., Fujii, L., Hedemark, B., & Chang, L.-H. (2009) · Neurology · doi:10.1212/01.wnl.0000346516.49126.20 · Cited by 80 · see citing works
Abnormal Hippocampal Neurochemistry in Smokers
Gallinat, J., Lang, U. E., Jacobsen, L. K., Bajbouj, M., Kalus, P., von Haebler, D., Seifert, F. C., & Schubert, F. (2007) · Journal of Clinical Psychopharmacology · doi:10.1097/jcp.0b013e31802dffde · Cited by 69 · see citing works
Magnetic Resonance Imaging Studies of Cigarette Smoking
Azizian, A., Monterosso, J. R., O’Neill, J., & London, E. D. (2009) · Handbook of experimental pharmacology · doi:10.1007/978-3-540-69248-5_5 · Cited by 67 · see citing works
Self-citationThe human brain : in photographs and diagrams
Nolte, J., & Angevine, J. B. (2013) · Cited by 62 · see citing works
Lim, K. O., Ardekani, B. A., Nierenberg, J. J., Butler, P. D., Javitt, D. C., & Hoptman, M. J. (2006) · American Journal of Psychiatry · doi:10.1176/ajp.2006.163.11.2008 · Cited by 61 · see citing works
Zhang, X., Stein, E. A., & Hong, L. E. (2010) · Biological Psychiatry · doi:10.1016/j.biopsych.2010.06.018 · Cited by 56 · see citing works
Fluorine-18-FPH for PET imaging of nicotinic acetylcholine receptors.
Horti, A. G., Scheffel, U., Stathis, M. J., et al. (1997) · PubMed · Cited by 55 · see citing works
The Human Brain: in photographs and diagrams
Allen, C. H. (1995) · Journal of Neurology Neurosurgery & Psychiatry · doi:10.1136/jnnp.59.3.345 · Cited by 55 · see citing works
Effect of nicotine on cerebellar granule neuron development
Opanashuk, L. A., Pauly, J. R., & Hauser, K. F. (2001) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2001.01359.x · Cited by 51 · see citing works
Wang, J. J., Durazzo, T. C., Gazdzinski, S. P., Yeh, P., Mon, A., & Meyerhoff, D. J. (2009) · NMR in Biomedicine · doi:10.1002/nbm.1363 · Cited by 50 · see citing works
Garrido, R., King‐Pospisil, K., Son, K. W., et al. (2003) · Neuroscience Research · doi:10.1016/s0168-0102(03)00222-0 · Cited by 47 · see citing works
Acetylcholinesterase inhibitors may improve myelin integrity
Bartzokis, G. (2007) · Biological Psychiatry · doi:10.1016/j.biopsych.2006.08.020 · Cited by 41 · see citing works
Self-citationLiu, J., Mohila, C., Gong, Y., Govindarajan, N., & Onn, S. (2005) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2005.04423.x · Cited by 35 · see citing works
Lim, K. O. (2006) · American Journal of Psychiatry · doi:10.1176/appi.ajp.163.11.2008 · Cited by 25 · see citing works
Brain Volume: Age-Related Changes
Bartzokis, G., & Lu, P. H. (2009) · Elsevier eBooks · doi:10.1016/b978-008045046-9.00107-8 · Cited by 9 · see citing works
Self-citation
Flagged first, then by citations
Research works printed but not linked: 1
- First MB Spitzer RL Gibbon M Williams JBW 2002 Structured Clinical Interview for DSM-IV Axis I Disorders- Patient Edition (SCID-I/P, version 2.0)
Cited by
Sorted by citations
Neural circuitry of impaired emotion regulation in substance use disorders
Wilcox, C. E., Pommy, J. M., & Adinoff, B. (2016) · American Journal of Psychiatry · doi:10.1176/appi.ajp.2015.15060710 · Cited by 213 · see citing works
Moylan, S., Jacka, F. N., Pasco, J. A., & Berk, M. (2013) · Brain and Behavior · doi:10.1002/brb3.137 · Cited by 186 · see citing works
Worth the wait: effects of age of onset of marijuana use on white matter and impulsivity
Gruber, S. A., Dahlgren, M. K., Sagar, K. A., Gönenç, A., & Lukas, S. E. (2014) · Psychopharmacology · doi:10.1007/s00213-013-3326-z · Cited by 177 · see citing works
Pfefferbaum, A., Rosenbloom, M. J., Chu, W., Sassoon, S. A., Rohlfing, T., Pohl, K. M., Zahr, N. M., & Sullivan, E. V. (2014) · The Lancet Psychiatry · doi:10.1016/s2215-0366(14)70301-3 · Cited by 115 · see citing works
Kochunov, P., Glahn, D. C., Rowland, L. M., Olvera, R. L., Winkler, A., Yang, Y.-H., Sampath, H., Carpenter, W. T., Duggirala, R., Curran, J., et al. (2013) · Biological Psychiatry · doi:10.1016/j.biopsych.2012.10.002 · Cited by 118 · see citing works
Hampton, W. H., Hanik, I. M., & Olson, I. R. (2019) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2019.02.005 · Cited by 95 · see citing works
Lin, F., Wu, G., Zhu, L., & Lei, H. (2013) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2012.09.013 · Cited by 79 · see citing works
Gogliettino, A. R., Potenza, M. N., & Yip, S. W. (2016) · Drug and Alcohol Dependence · doi:10.1016/j.drugalcdep.2016.02.015 · Cited by 56 · see citing works
Low Smoking Exposure, the Adolescent Brain, and the Modulating Role of CHRNA5 Polymorphisms
Chaarani, B., Kan, K.-J., Mackey, S., Spechler, P. A., Potter, A., Orr, C., D’Alberto, N., Hudson, K. E., Banaschewski, T., Bokde, A. L. W., et al. (2019) · Biological Psychiatry: Cognitive Neuroscience and Neuroimaging · doi:10.1016/j.bpsc.2019.02.006 · Cited by 32 · see citing works
Wang, S., Zuo, L., Jiang, T., Peng, P., Chu, S., & Xiao, D. (2017) · Neurological Research · doi:10.1080/01616412.2017.1379277 · Cited by 12 · see citing works
Shen, Q., Heikkinen, N., Kärkkäinen, O., Gröhn, H., Könönen, M., Liu, Y., Kaarre, O., Zhang, Z., Tan, C., Tolmunen, T., et al. (2019) · Psychiatry Research: Neuroimaging · doi:10.1016/j.pscychresns.2019.111003 · Cited by 11 · see citing works
- Authors
- Hudkins, M., O’Neill, J., Tobias, M. C., Bartzokis, G., & London, E. D.
- Affiliations
- University of California, Los Angeles (US)
- Corresponding author
- O’Neill, Joseph
- Venue
- Psychopharmacology
- Published
- 2012-01-04
- Volume
- 221
- Issue
- 2
- Pages
- 285-295
- ISSN
- 0033-3158 (ISSN-L)
- 1432-2072
- PMC
- PMC4111107
- OpenAlex
- W1964156407
- Cited by
- 95
- References
- 54
- Citations by year
- 2026: 2 · 2025: 2 · 2024: 6 · 2023: 5 · 2022: 8 · 2021: 7 · 2020: 5 · 2019: 8 · 2018: 7 · 2017: 10 · 2016: 7 · 2015: 5 · 2014: 12 · 2013: 6 · 2012: 5
- FWCI
- 6.76
- Type
- journal article
- Language
- en
- Open access
- green
- www.ncbi.nlm.nih.gov
- Licence
- www.springer.com/tdm (tdm)
- Locations
- Psychopharmacology (publishedVersion)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- Funders
- U.S. Public Health Service (MOIRR00865)
- National Institute on Drug Abuse (R03 DA20512, P20DA022539, R03DA020512, R21DA023192, R01DA020726)
- National Center for Research Resources (M01RR000865)
- Topics
- Health Sciences › Medicine › Radiology, Nuclear Medicine and Imaging › Advanced Neuroimaging Techniques and Applications
- Health Sciences › Medicine › Physiology › Smoking Behavior and Cessation
- Health Sciences › Medicine › Pediatrics, Perinatology and Child Health › Prenatal Substance Exposure Effects
- Keywords
- cigarette smoking, white matter microstructure, fractional anisotropy, apparent diffusion coefficient, nicotine dependence, corpus callosum, prefrontal white matter, cingulum, diffusion tensor imaging, pack-years
- MeSH terms
- Adult, Age Factors, Brain, Brain Mapping, Cross-Sectional Studies, Female, Humans, Male, Middle Aged, Smoking, Case-Control Studies, Anisotropy, Young Adult, Diffusion Tensor Imaging
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