Hostname: page-component-848d4c4894-ndmmz Total loading time: 0 Render date: 2024-05-14T14:11:08.497Z Has data issue: false hasContentIssue false

Analysis of the superior temporal gyrus as a possible biomarker in schizophrenia using voxel-based morphometry of the brain magnetic resonance imaging: a comprehensive review

Published online by Cambridge University Press:  10 January 2020

Igor D. Bandeira*
Affiliation:
Laboratory of Neuropsychopharmacology, Federal University of Bahia, Salvador, Brazil Postgraduate Program in Medicine and Health, Medical School of Bahia, Federal University of Bahia, Salvador, Brazil
Judah L. Barouh
Affiliation:
Laboratory of Neuromodulation & Center for Clinical Research Learning, Physics and Rehabilitation Department, Spaulding Rehabilitation Hospital, Harvard Medical School, Boston, Massachusetts, USA
Ingrid D. Bandeira
Affiliation:
Department of Medicine, Faculty of Science and Technology, Salvador, Brazil
Lucas Quarantini
Affiliation:
Laboratory of Neuropsychopharmacology, Federal University of Bahia, Salvador, Brazil Department of Neuroscience and Mental Health, Medical School of Bahia, Federal University of Bahia, Salvador, Brazil
*
*Igor D. Bandeira, Email: igordbandeira@gmail.com

Abstract

The lack of predictive biomarkers for therapeutic responses to schizophrenia leads clinical procedures to be decided without taking into account the subjects’ neuroanatomical features, a consideration, which could help in identifying specific pharmacological treatments for the remission of symptoms. Magnetic resonance imaging (MRI) is a technique widely used for radiological diagnosis and produces 3-dimensional images in excellent anatomical detail, and with a great capacity to differentiate soft tissue. Various MRI techniques of the human brain have emerged as a result of research, enabling structural tests that may help to in consolidate previous findings and lead to the discovery of new patterns of abnormality in schizophrenia. A literature review was undertaken to assess the superior temporal gyrus (STG) as a possible biomarker in schizophrenia with the use of voxel-based morphometry of the brain using MRI. Many findings in studies of schizophrenia using MRI have been inconclusive and, in some cases, conflicting, although interesting results have been obtained when attempting to correlate neuroimaging changes with aspects of clinical features and prognosis of the disease. The individuals affected by this mental illness appear to have smaller STG volumes when compared to healthy controls and also to subjects with a diagnosis of first-episode affective psychosis or groups of individuals at high risk of psychosis. However, the wide variety of definitions surrounding the STG found in a number of studies is a contributing factor to the lack of correlation between brain abnormalities and clinical symptoms. For instance, disagreements have arisen due to studies using regions of interest to analyze the STG whereas other studies prioritize the analysis of only STG subregions or specific supratemporal plane regions. It is necessary to standardize the nomenclature of the areas to be studied in the future, as this will enable more consistent results, allowing higher clinical and morphological correlations.

Type
Perspective
Copyright
© Cambridge University Press 2020

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

Madre, M, Canales-Rodriguez, EJ, Ortiz-Gil, J, et al. Neuropsychological and neuroimaging underpinnings of schizoaffective disorder: a systematic review. Acta Psychiatr Scand. 2016;134 (1):1630.10.1111/acps.12564CrossRefGoogle ScholarPubMed
Rinaldi, R, Lefebvre, L. Goal-directed behaviors in patients with schizophrenia: concept relevance and updated model. Psychiatry Clin Neurosci. 2016;70 (9):394404.CrossRefGoogle ScholarPubMed
McGrath, J, Saha, S, Welham, J, El Saadi, O, MacCauley, C, Chant, D. A systematic review of the incidence of schizophrenia: the distribution of rates and the influence of sex, urbanicity, migrant status and methodology. BMC Med. 2004;2:13.CrossRefGoogle ScholarPubMed
Marwaha, S, Johnson, S. Schizophrenia and employment—a review. Soc Psychiatry Psychiatr Epidemiol. 2004;39 (5):337349.CrossRefGoogle Scholar
Bobes, J, Garcia-Portilla, MP, Bascaran, MT, Saiz, PA, Bousono, M. Quality of life in schizophrenic patients. Dialog Clin Neurosci. 2007;9 (2):215226.CrossRefGoogle ScholarPubMed
Kooyman, I, Dean, K, Harvey, S, Walsh, E. Outcomes of public concern in schizophrenia. Br J Psychiatry Suppl. 2007;50:s29s36.10.1192/bjp.191.50.s29CrossRefGoogle Scholar
Boter, H, Peuskens, J, Libiger, J, et al. Effectiveness of antipsychotics in first-episode schizophrenia and schizophreniform disorder on response and remission: an open randomized clinical trial (EUFEST). Schizophr Res. 2009;115(2–3):97103.10.1016/j.schres.2009.09.019CrossRefGoogle Scholar
Dazzan, P, Arango, C, Fleischacker, W, et al. Magnetic resonance imaging and the prediction of outcome in first-episode schizophrenia: a review of current evidence and directions for future research. Schizophr Bull. 2015;41 (3):574583.CrossRefGoogle ScholarPubMed
Boksa, P. A way forward for research on biomarkers for psychiatric disorders. J Psychiatry Neurosci. 2013;38 (2):7577.10.1503/jpn.130018CrossRefGoogle ScholarPubMed
Aberg, KA, McClay, JL, Nerella, S, et al. Methylome-wide association study of schizophrenia: identifying blood biomarker signatures of environmental insults. JAMA Psychiatry. 2014;71 (3):255264.10.1001/jamapsychiatry.2013.3730CrossRefGoogle ScholarPubMed
Liu, J, Chen, J, Ehrlich, S, et al. Methylation patterns in whole blood correlate with symptoms in schizophrenia patients. Schizophr Bull. 2014;40 (4):769776.10.1093/schbul/sbt080CrossRefGoogle ScholarPubMed
Alam, MA, Lin, HY, Deng, HW, Calhoun, VD, Wang, YP. A kernel machine method for detecting higher order interactions in multimodal datasets: application to schizophrenia. J Neurosci Methods. 2018;309:161174.10.1016/j.jneumeth.2018.08.027CrossRefGoogle Scholar
Gore, JC. Principles and practice of functional MRI of the human brain. J Clin Investig. 2003;112 (1):49.10.1172/JCI200319010CrossRefGoogle ScholarPubMed
Nelson, MD, Saykin, AJ, Flashman, LA, Riordan, HJ. Hippocampal volume reduction in schizophrenia as assessed by magnetic resonance imaging: a meta-analytic study. Arch Gen Psychiatry. 1998;55 (5):433440.CrossRefGoogle ScholarPubMed
Wright, IC, Rabe-Hesketh, S, Woodruff, PW, David, AS, Murray, RM, Bullmore, ET. Meta-analysis of regional brain volumes in schizophrenia. Am J Psychiatry. 2000;157 (1):1625.CrossRefGoogle Scholar
Del Re, EC, Konishi, J, Bouix, S, et al. Enlarged lateral ventricles inversely correlate with reduced corpus callosum central volume in first episode schizophrenia: association with functional measures. Brain Imaging Behav. 2016;10 (4):12641273.CrossRefGoogle ScholarPubMed
Ashburner, J, Friston, KJ. Voxel-based morphometry—the methods. NeuroImage. 2000;11(6 Pt 1):805821.10.1006/nimg.2000.0582CrossRefGoogle Scholar
Wolkin, A, Rusinek, H, Vaid, G, et al. Structural magnetic resonance image averaging in schizophrenia. Am J Psychiatry. 1998;155 (8):10641073.10.1176/ajp.155.8.1064CrossRefGoogle Scholar
Kubicki, M, Shenton, ME, Salisbury, DF, et al. Voxel-based morphometric analysis of gray matter in first episode schizophrenia. NeuroImage. 2002;17 (4):17111719.10.1006/nimg.2002.1296CrossRefGoogle ScholarPubMed
Kambeitz, J, Kambeitz-Ilankovic, L, Leucht, S, et al. Detecting neuroimaging biomarkers for schizophrenia: a meta-analysis of multivariate pattern recognition studies. Neuropsychopharmacology. 2015;40 (7):17421751.10.1038/npp.2015.22CrossRefGoogle ScholarPubMed
Scarr, E, Millan, MJ, Bahn, S, et al. Biomarkers for psychiatry: the journey from fantasy to fact, a report of the 2013 CINP think tank. Int J Neuropsychopharmacol. 2015;18 (10):pyv042.10.1093/ijnp/pyv042CrossRefGoogle ScholarPubMed
Bandeira, ID, Mendoza, J. Medical education and leadership: a call to action for Brazil’s mental health system. Int J Med Educ. 2018;9:170172.CrossRefGoogle Scholar
Johnstone, EC, Owens, DG, Crow, TJ, et al. Temporal lobe structure as determined by nuclear magnetic resonance in schizophrenia and bipolar affective disorder. J Neurol Neurosurg Psychiatry. 1989;52 (6):736741.CrossRefGoogle ScholarPubMed
Suddath, RL, Casanova, MF, Goldberg, TE, Daniel, DG, Kelsoe, JR Jr, Weinberger, DR. Temporal lobe pathology in schizophrenia: a quantitative magnetic resonance imaging study. Am J Psychiatry. 1989;146 (4):464472.Google ScholarPubMed
Penfield, W, Perot, P. The brain’s record of auditory and visual experience. A final summary and discussion. Brain. 1963;86:595696.CrossRefGoogle ScholarPubMed
Barta, PE, Pearlson, GD, Powers, RE, Richards, SS, Tune, LE. Auditory hallucinations and smaller superior temporal gyral volume in schizophrenia. Am J Psychiatry. 1990;147 (11):14571462.Google Scholar
Zipursky, RB, Marsh, L, Lim, KO, et al. Volumetric MRI assessment of temporal lobe structures in schizophrenia. Biol Psychiatry. 1994;35 (8):501516.10.1016/0006-3223(94)90097-3CrossRefGoogle Scholar
Vita, A, Dieci, M, Giobbio, GM, et al. Language and thought disorder in schizophrenia: brain morphological correlates. Schizophr Res. 1995;15 (3):243251.CrossRefGoogle ScholarPubMed
Spalthoff, R, Gaser, C, Nenadic, I. Altered gyrification in schizophrenia and its relation to other morphometric markers. Schizophr Res. 2018;202:195202.10.1016/j.schres.2018.07.014CrossRefGoogle ScholarPubMed
Ananth, H, Popescu, I, Critchley, HD, Good, CD, Frackowiak, RS, Dolan, RJ. Cortical and subcortical gray matter abnormalities in schizophrenia determined through structural magnetic resonance imaging with optimized volumetric voxel-based morphometry. Am J Psychiatry. 2002;159 (9):14971505.10.1176/appi.ajp.159.9.1497CrossRefGoogle ScholarPubMed
Barta, PE, Pearlson, GD, Brill, LB, et al. Planum temporale asymmetry reversal in schizophrenia: replication and relationship to gray matter abnormalities. Am J Psychiatry. 1997;154 (5):661667.Google ScholarPubMed
Pearlson, GD, Barta, PE, Powers, RE, et al. Ziskind-Somerfeld Research Award 1996. Medial and superior temporal gyral volumes and cerebral asymmetry in schizophrenia versus bipolar disorder. Biol Psychiatry. 1997;41 (1):114.CrossRefGoogle ScholarPubMed
Sanfilipo, M, Lafargue, T, Rusinek, H, et al. Volumetric measure of the frontal and temporal lobe regions in schizophrenia: relationship to negative symptoms. Archiv Gen Psychiatry. 2000;57 (5):471480.10.1001/archpsyc.57.5.471CrossRefGoogle ScholarPubMed
Matsumoto, H, Simmons, A, Williams, S, et al. Superior temporal gyrus abnormalities in early-onset schizophrenia: similarities and differences with adult-onset schizophrenia. Am J Psychiatry. 2001;158 (8):12991304.CrossRefGoogle ScholarPubMed
Shapleske, J, Rossell, SL, Chitnis, XA, et al. A computational morphometric MRI study of schizophrenia: effects of hallucinations. Cereb Cortex. 2002;12 (12):13311341.CrossRefGoogle ScholarPubMed
Neckelmann, G, Specht, K, Lund, A, et al. Mr morphometry analysis of grey matter volume reduction in schizophrenia: association with hallucinations. Int J Neurosci. 2006;116 (1):923.CrossRefGoogle ScholarPubMed
Modinos, G, Vercammen, A, Mechelli, A, Knegtering, H, McGuire, PK, Aleman, A. Structural covariance in the hallucinating brain: a voxel-based morphometry study. J Psychiatry Neurosci. 2009;34 (6):465469.Google ScholarPubMed
Nenadic, I, Smesny, S, Schlosser, RG, Sauer, H, Gaser, C. Auditory hallucinations and brain structure in schizophrenia: voxel-based morphometric study. Br J Psychiatry. 2010;196 (5):412413.CrossRefGoogle ScholarPubMed
van Tol, MJ, van der Meer, L, Bruggeman, R, Modinos, G, Knegtering, H, Aleman, A. Voxel-based gray and white matter morphometry correlates of hallucinations in schizophrenia: the superior temporal gyrus does not stand alone. Neuroimage Clin. 2014;4:249257.CrossRefGoogle Scholar
Hirayasu, Y, Shenton, ME, Salisbury, DF, et al. Lower left temporal lobe MRI volumes in patients with first-episode schizophrenia compared with psychotic patients with first-episode affective disorder and normal subjects. Am J Psychiatry. 1998;155 (10):13841391.CrossRefGoogle ScholarPubMed
Gur, RE, Turetsky, BI, Cowell, PE, et al. Temporolimbic volume reductions in schizophrenia. Archiv Gen Psychiatry. 2000;57 (8):769775.CrossRefGoogle Scholar
Hulshoff Pol, HE, Schnack, HG, Mandl, RC, et al. Focal gray matter density changes in schizophrenia. Archiv Gen Psychiatry. 2001;58 (12):11181125.CrossRefGoogle Scholar
Shenton, ME, Kikinis, R, Jolesz, FA, et al. Abnormalities of the left temporal lobe and thought disorder in schizophrenia. A quantitative magnetic resonance imaging study. New Engl J Med. 1992;327 (9):604612.CrossRefGoogle ScholarPubMed
Sumich, A, Chitnis, XA, Fannon, DG, et al. Unreality symptoms and volumetric measures of Heschl’s gyrus and planum temporal in first-episode psychosis. Biol Psychiatry. 2005;57 (8):947950.CrossRefGoogle ScholarPubMed
Hasan, A, Kremer, L, Gruber, O, et al. Planum temporale asymmetry to the right hemisphere in first-episode schizophrenia. Psychiatry Res. 2011;193 (1):5659.10.1016/j.pscychresns.2011.02.008CrossRefGoogle Scholar
Flaum, M, O’Leary, DS, Swayze, VW, Miller, DD, Arndt, S, Andreasen, NC. Symptom dimensions and brain morphology in schizophrenia and related psychotic disorders. J Psychiatr Res. 1995;29 (4):261276.CrossRefGoogle ScholarPubMed
Menon, RR, Barta, PE, Aylward, EH, et al. Posterior superior temporal gyrus in schizophrenia: grey matter changes and clinical correlates. Schizophr Res. 1995;16 (2):127135.CrossRefGoogle ScholarPubMed
Kim, JJ, Crespo-Facorro, B, Andreasen, NC, O’Leary, DS, Magnotta, V, Nopoulos, P. Morphology of the lateral superior temporal gyrus in neuroleptic nai;ve patients with schizophrenia: relationship to symptoms. Schizophr Res. 2003;60(2–3):173181.Google ScholarPubMed
Ohi, K, Matsuda, Y, Shimada, T, et al. Structural alterations of the superior temporal gyrus in schizophrenia: detailed subregional differences. Eur Psychiatry. 2016;35:2531.CrossRefGoogle ScholarPubMed
Escarti, MJ, Garcia-Marti, G, Sanz-Requena, R, et al. Auditory hallucinations in first-episode psychosis: a voxel-based morphometry study. Schizophr Res. 2019;209:148155.CrossRefGoogle ScholarPubMed
Plaze, M, Paillere-Martinot, ML, Penttila, J, et al. “Where do auditory hallucinations come from?”—a brain morphometry study of schizophrenia patients with inner or outer space hallucinations. Schizophr Bull. 2011;37 (1):212221.10.1093/schbul/sbp081CrossRefGoogle ScholarPubMed
Nenadic, I, Sauer, H, Gaser, C. Distinct pattern of brain structural deficits in subsyndromes of schizophrenia delineated by psychopathology. NeuroImage. 2010;49 (2):11531160.10.1016/j.neuroimage.2009.10.014CrossRefGoogle ScholarPubMed
O’Daly, OG, Frangou, S, Chitnis, X, Shergill, SS. Brain structural changes in schizophrenia patients with persistent hallucinations. Psychiatry Res. 2007;156 (1):1521.10.1016/j.pscychresns.2007.03.001CrossRefGoogle ScholarPubMed
Xiao, P, Dai, Z, Zhong, J, Zhu, Y, Shi, H, Pan, P. Regional gray matter deficits in alcohol dependence: a meta-analysis of voxel-based morphometry studies. Drug Alcohol Depend. 2015;153:2228.CrossRefGoogle ScholarPubMed
Quinn, M, McHugo, M, Armstrong, K, Woodward, N, Blackford, J, Heckers, S. Impact of substance use disorder on gray matter volume in schizophrenia. Psychiatry Res Neuroimaging. 2018;280:914.10.1016/j.pscychresns.2018.08.002CrossRefGoogle Scholar
Malchow, B, Hasan, A, Schneider-Axmann, T, et al. Effects of cannabis and familial loading on subcortical brain volumes in first-episode schizophrenia. Eur Arch Psychiatry Clin Neurosci. 2013;263(Suppl 2):S155S168.CrossRefGoogle ScholarPubMed
Thoma, P, Daum, I. Comorbid substance use disorder in schizophrenia: a selective overview of neurobiological and cognitive underpinnings. Psychiatry Clin Neurosci. 2013;67 (6):367383.CrossRefGoogle ScholarPubMed
DeLisi, LE, Sakuma, M, Tew, W, Kushner, M, Hoff, AL, Grimson, R. Schizophrenia as a chronic active brain process: a study of progressive brain structural change subsequent to the onset of schizophrenia. Psychiatry Res. 1997;74 (3):129140.CrossRefGoogle Scholar
Hulshoff Pol, HE, Schnack, HG, Bertens, MG, et al. Volume changes in gray matter in patients with schizophrenia. Am J Psychiatry. 2002;159 (2):244250.CrossRefGoogle ScholarPubMed
Fusar-Poli, P, Bonoldi, I, Yung, AR, et al. Predicting psychosis: meta-analysis of transition outcomes in individuals at high clinical risk. Archiv Gen Psychiatry. 2012;69 (3):220229.10.1001/archgenpsychiatry.2011.1472CrossRefGoogle ScholarPubMed
Job, DE, Whalley, HC, McConnell, S, Glabus, M, Johnstone, EC, Lawrie, SM. Voxel-based morphometry of grey matter densities in subjects at high risk of schizophrenia. Schizophr Res. 2003;64 (1):113.CrossRefGoogle ScholarPubMed
Ziermans, TB, Schothorst, PF, Schnack, HG, et al. Progressive structural brain changes during development of psychosis. Schizophr Bull. 2012;38 (3):519530.CrossRefGoogle Scholar
Mechelli, A, Riecher-Rossler, A, Meisenzahl, EM, et al. Neuroanatomical abnormalities that predate the onset of psychosis: a multicenter study. Archiv Gen Psychiatry. 2011;68 (5):489495.CrossRefGoogle ScholarPubMed
Witthaus, H, Kaufmann, C, Bohner, G, et al. Gray matter abnormalities in subjects at ultra-high risk for schizophrenia and first-episode schizophrenic patients compared to healthy controls. Psychiatry Res. 2009;173 (3):163169.CrossRefGoogle ScholarPubMed
Cannon, TD, Chung, Y, He, G, et al. Progressive reduction in cortical thickness as psychosis develops: a multisite longitudinal neuroimaging study of youth at elevated clinical risk. Biol Psychiatry. 2015;77 (2):147157.CrossRefGoogle ScholarPubMed
Benetti, S, Pettersson-Yeo, W, Hutton, C, et al. Elucidating neuroanatomical alterations in the At Risk Mental State and first episode psychosis: a combined voxel-based morphometry and voxel-based cortical thickness study. Schizophr Res. 2013;150(2–3):505511.CrossRefGoogle ScholarPubMed
Koutsouleris, N, Meisenzahl, EM, Davatzikos, C, et al. Use of neuroanatomical pattern classification to identify subjects in at-risk mental states of psychosis and predict disease transition. Archiv Gen Psychiatry. 2009;66 (7):700712.CrossRefGoogle ScholarPubMed
Chin, R, You, AX, Meng, F, Zhou, J, Sim, K. Recognition of schizophrenia with regularized support vector machine and sequential region of interest selection using structural magnetic resonance imaging. Sci Rep. 2018;8 (1):13858.10.1038/s41598-018-32290-9CrossRefGoogle ScholarPubMed
Vyskovsky, R, Schwarz, D, Kasparek, T. Brain morphometry methods for feature extraction in random subspace ensemble neural network classification of first-episode schizophrenia. Neural Comput. 2019;31 (5):897918.CrossRefGoogle ScholarPubMed
Kasai, K, Shenton, ME, Salisbury, DF, et al. Progressive decrease of left superior temporal gyrus gray matter volume in patients with first-episode schizophrenia. Am J Psychiatry. 2003;160 (1):156164.CrossRefGoogle ScholarPubMed
Rao, JS, Kim, HW, Harry, GJ, Rapoport, SI, Reese, EA. RETRACTED: increased neuroinflammatory and arachidonic acid cascade markers, and reduced synaptic proteins, in the postmortem frontal cortex from schizophrenia patients. Schizophr Res. 2013;147 (1):2431.CrossRefGoogle ScholarPubMed
Milatovic, D, Gupta, RC, Yu, Y, Zaja-Milatovic, S, Aschner, M. Protective effects of antioxidants and anti-inflammatory agents against manganese-induced oxidative damage and neuronal injury. Toxicol Appl Pharmacol. 2011;256 (3):219226.CrossRefGoogle ScholarPubMed
Bandeira, ID, Guimaraes, RS, Jagersbacher, JG, et al. Transcranial direct current stimulation in children and adolescents with Attention-Deficit/Hyperactivity Disorder (ADHD): a pilot study. J Child Neurol. 2016;31 (7):918924.CrossRefGoogle ScholarPubMed
Barretto, TL, Bandeira, ID, Jagersbacher, JG, et al. Transcranial direct current stimulation in the treatment of cerebellar ataxia: a two-phase, double-blind, auto-matched, pilot study. Clin Neurol Neurosurg. 2019;182:123129.CrossRefGoogle ScholarPubMed
Rios, DM, Correia Rios, M, Bandeira, ID, Queiros Campbell, F, de Carvalho Vaz, D, Lucena, R. Impact of transcranial direct current stimulation on reading skills of children and adolescents with dyslexia. Child Neurol Open. 2018;5:2329048.CrossRefGoogle ScholarPubMed
Correia-Melo, FS, Leal, GC, Carvalho, MS, et al. Comparative study of esketamine and racemic ketamine in treatment-resistant depression: protocol for a non-inferiority clinical trial. Medicine. 2018;97 (38):e12414.CrossRefGoogle ScholarPubMed
Tomasetti, C, Montemitro, C, Fiengo, ALC, et al. Novel pathways in the treatment of major depression: focus on the glutamatergic system. Curr Pharm Des. 2019;25 (4):381387.CrossRefGoogle ScholarPubMed
Premoli, M, Aria, F, Bonini, SA, et al. Cannabidiol: recent advances and new insights for neuropsychiatric disorders treatment. Life Sci. 2019;224:120127.CrossRefGoogle ScholarPubMed
Correia-Melo, FS, Leal, GC, Vieira, F, et al. Efficacy and safety of adjunctive therapy using esketamine or racemic ketamine for adult treatment-resistant depression: A randomized, double-blind, non-inferiority study [published online ahead of print, 2019 Nov 14]. J Affect Disord. 2019;S0165–0327(19)31978–0. doi:10.1016/j.jad.2019.11.086.Google ScholarPubMed
Barreto, TM, Bento, MN, Barreto, TM, et al. Prevalence of depression, anxiety, and substance-related disorders in parents of children with cerebral palsy: a systematic review. Dev Med Child Neurol. 2019. doi:10.1111/dmcn.14321.Google ScholarPubMed
Kessler, RC, Aguilar-Gaxiola, S, Alonso, J, et al. The global burden of mental disorders: an update from the WHO World Mental Health (WMH) surveys. Epidemiol Psichiatr Soc. 2009;18 (1):2333.CrossRefGoogle ScholarPubMed