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Evaluation of structural connectivity changes in betel-quid chewers using generalized q-sampling MRI

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Abstract

Rationale

Betel quid (BQ) is a common addictive substance in many Asian countries. However, few studies have focused on the influences of BQ on the brain. It remains unclear how BQ can affect structural brain abnormalities in BQ chewers.

Objectives

We aimed to use generalized q-sampling imaging (GQI) to evaluate the impact of the neurological structure of white matter caused by BQ.

Methods

The study population comprised 16 BQ chewers, 15 tobacco and alcohol controls, and 17 healthy controls. We used GQI with voxel-based statistical analysis (VBA) to evaluate structural brain and connectivity abnormalities in the BQ chewers compared to the tobacco and alcohol controls and the healthy controls. Graph theoretical analysis (GTA) and network-based statistical (NBS) analysis were also performed to identify the structural network differences among the three groups.

Results

Using GQI, we found increases in diffusion anisotropy in the right anterior cingulate cortex (ACC), the midbrain, the bilateral angular gyrus, the right superior temporal gyrus (rSTG), the bilateral superior occipital gyrus, the left middle occipital gyrus, the bilateral superior and inferior parietal lobule, and the bilateral postcentral and precentral gyrus in the BQ chewers when compared to the tobacco and alcohol controls and the healthy controls. In GTA and NBS analyses, we found more connections in connectivity among the BQ chewers, particularly in the bilateral anterior cingulum.

Conclusions

Our results provided further evidence indicating that BQ chewing may lead to brain structure and connectivity changes in BQ chewers.

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References

  • Bales A, Peterson MJ, Ojha S, Upadhaya K, Adhikari B, Barrett B (2009) Associations between betel nut (Areca catechu) and symptoms of schizophrenia among patients in Nepal: a longitudinal study. Psychiatry Res 169:203–211

    Article  PubMed  Google Scholar 

  • Benegal V, Rajkumar RP, Muralidharan K (2008) Does areca nut use lead to dependence? Drug Alcohol Depend 97:114–121

    Article  PubMed  Google Scholar 

  • Bigler ED, Mortensen S, Neeley ES, Ozonoff S, Krasny L, Johnson M, Lu J, Provencal SL, McMahon W, Lainhart JE (2007) Superior temporal gyrus, language function, and autism. Dev Neuropsychol 31:217–238

    Article  PubMed  Google Scholar 

  • Blood AJ, Iosifescu DV, Makris N, Perlis RH, Kennedy DN, Dougherty DD, Kim BW, Lee MJ, Wu S, Lee S, Calhoun J, Hodge SM, Fava M, Rosen BR, Smoller JW, Gasic GP, Breiter HC, Phenotype Genotype Project on Addiction and Mood Disorder (2010) Microstructural abnormalities in subcortical reward circuitry of subjects with major depressive disorder. PLoS One 5:e13945

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Buckner RL, Andrews-Hanna JR, Schacter DL (2008) The brain’s default network. Ann N Y Acad Sci 1124:1–38

    Article  PubMed  Google Scholar 

  • Bullmore ET, Bassett DS (2011) Brain graphs: graphical models of the human brain connectome. Annu Rev Clin Psychol 7:113–140

    Article  PubMed  Google Scholar 

  • Bullmore E, Sporns O (2009) Complex brain networks: graph theoretical analysis of structural and functional systems. Nat Rev Neurosci 10:186–198

    Article  CAS  PubMed  Google Scholar 

  • Chen CH, Chen WJ, Cheng AT (2005) New approach to the validity of the Alcohol Use Disorders Identification Test: stratum-specific likelihood ratios analysis. Alcohol Clin Exp Res 29:602–608

    Article  PubMed  Google Scholar 

  • Chen F, Zhong Y, Zhang Z, Xu Q, Liu T, Pan M, Li J, Lu G (2015) Gray matter abnormalities associated with betel quid dependence: a voxel-based morphometry study. Am J Transl Res 7:364–374

    CAS  PubMed  PubMed Central  Google Scholar 

  • Chen VC, Shen CY, Liang SH, Li ZH, Tyan YS, Liao YT, Huang YC, Lee Y, McIntyre RS, Weng JC (2016) Assessment of abnormal brain structures and networks in major depressive disorder using morphometric and connectome analyses. J Affect Disord 205:103–111

    Article  PubMed  Google Scholar 

  • Cheng Y, Xu J, Yu H, Nie B, Li N, Luo C, Li H, Liu F, Bai Y, Shan B, Xu L, Xu X (2014) Delineation of early and later adult onset depression by diffusion tensor imaging. PLoS One 9:e112307

    Article  PubMed  PubMed Central  Google Scholar 

  • Chu NS (2002) Neurological aspects of areca and betel chewing. Addict Biol 7:111–114

    Article  PubMed  Google Scholar 

  • Chuang C, Chang C, Chang C (2007) The workplace relevant factors of betel quid chewing among transportation workers in central Taiwan. Taiwan Public Health 26:433–442

    Google Scholar 

  • Ersche KD, Jones PS, Williams GB, Turton AJ, Robbins TW, Bullmore ET (2012) Abnormal brain structure implicated in stimulant drug addiction. Science 335:601–604

    Article  CAS  PubMed  Google Scholar 

  • Ersche KD, Jones PS, Williams GB, Smith DG, Bullmore ET, Robbins TW (2013a) Distinctive personality traits and neural correlates associated with stimulant drug use versus familial risk of stimulant dependence. Biol Psychiatry 74:137–144

    Article  PubMed  PubMed Central  Google Scholar 

  • Ersche KD, Williams GB, Robbins TW, Bullmore ET (2013b) Meta-analysis of structural brain abnormalities associated with stimulant drug dependence and neuroimaging of addiction vulnerability and resilience. Curr Opin Neurobiol 23:615–624

    Article  CAS  PubMed  Google Scholar 

  • Everitt BJ, Parkinson JA, Olmstead MC, Arroyo M, Robledo P, Robbins TW (1999) Associative processes in addiction and reward the role of amygdala-ventral striatal subsystems. Ann N Y Acad Sci 877:412–438

    Article  CAS  PubMed  Google Scholar 

  • Fagerström K-O (1978) Measuring degree of physical dependence to tobacco smoking with reference to individualization of treatment. Addict Behav 3:235–241

    Article  PubMed  Google Scholar 

  • Fornito A, Zalesky A, Bullmore ET (2010) Network scaling effects in graph analytic studies of human resting-state FMRI data. Front Syst Neurosci 4:22

    PubMed  PubMed Central  Google Scholar 

  • Goldstein RZ, Bechara A, Garavan H, Childress AR, Paulus MP, Volkow ND (2009) The neurocircuitry of impaired insight in drug addiction. Trends Cogn Sci 13:372–380

    Article  PubMed  PubMed Central  Google Scholar 

  • Gong Q, He Y (2015) Depression, neuroimaging and connectomics: a selective overview. Biol Psychiatry 77:223–235

    Article  PubMed  Google Scholar 

  • Greicius MD, Krasnow B, Reiss AL, Menon V (2003) Functional connectivity in the resting brain: a network analysis of the default mode hypothesis. Proc Natl Acad Sci 100:253–258

    Article  CAS  PubMed  Google Scholar 

  • Gupta PC, Ray CS (2004) Epidemiology of betel quid usage. Ann Acad Med Singap 33:31–36

    CAS  PubMed  Google Scholar 

  • Heatherton TF, Wagner DD (2011) Cognitive neuroscience of self-regulation failure. Trends Cogn Sci 15:132–139

    Article  PubMed  PubMed Central  Google Scholar 

  • Ho MC, Wang CK (2010) Can betel nut chewing affect the UFOV size after sleep deprivation? Chinese Journal of Psychology 52:445–456

    Google Scholar 

  • Ho MC, Wang CK (2011) The effect of betel nut chewing on contour and object masking. Attention, Perception & Psychophysics 73:2583–2593

    Article  Google Scholar 

  • Ho MC, Li RH, Tang TC (2015) Betel nut chewing effects on sustained attention and inhibitory control after sleep deprivation. Aust J Psychol 67:222–230

    Article  Google Scholar 

  • Hosseini SM, Hoeft F, Kesler SR (2012) GAT: a graph-theoretical analysis toolbox for analyzing between-group differences in large-scale structural and functional brain networks. PLoS One 7:e40709

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang C-L, Lin H-H, Wang H-H (2006) The psychometric properties of the Chinese version of the Fagerstrom test for nicotine dependence. Addict Behav 31:2324–2327

    Article  PubMed  Google Scholar 

  • Huang X, Liu Z, Mwansisya TE, Pu W, Zhou L, Liu C, Chen X, Rohrbaugh R, Marienfeld C, Xue Z (2016) Betel quid chewing alters functional connectivity in frontal and default networks: a resting-state fMRI study. Journal of Magnetic Resonance Imaging.

  • IARC (2004) Betel-quid and areca-nut chewing and some areca-nut-derived nitrosamines IARC monographs on the evaluation of carcinogenic risks to humans, Lyon

  • Jensen JH, Helpern JA, Ramani A, Lu H, Kaczynski K (2005) Diffusional kurtosis imaging: the quantification of non-Gaussian water diffusion by means of magnetic resonance imaging. Magn Reson Med 53:1432–1440

    Article  PubMed  Google Scholar 

  • Jou RJ, Minshew NJ, Keshavan MS, Vitale MP, Hardan AY (2010) Enlarged right superior temporal gyrus in children and adolescents with autism. Brain Res 1360:205–212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Koob GF (2006) The neurobiology of addiction: a neuroadaptational view relevant for diagnosis. Addiction 101:23–30

    Article  PubMed  Google Scholar 

  • Koob GF, Volkow ND (2010) Neurocircuitry of addiction. Neuropsychopharmacology 35:217–238

    Article  PubMed  Google Scholar 

  • Lee CH, Chiang SL, Ko AMS, Hua CH, Tsai MH, Warnakulasuriya S, Ibrahim SO, Zain RB, Ling TY, Huang CL (2014) Betel-quid dependence domains and syndrome associated with betel-quid ingredients among chewers: an Asian multi-country evidence. Addiction 109:1194–1204

    Article  PubMed  Google Scholar 

  • Li RH, Ho MC, Tang TC, Chang CF (2012) Development of the Betel Nut Dependency Scale (BNDS). Chinese Journal of Psychology 54:331–348

    Google Scholar 

  • Liu T, Li J, Huang S, Zhao Z, Yang G, Pan M, Li C, Chen F, Pan S (2015) Neurochemical abnormalities in anterior cingulate cortex on betel quid dependence: a 2D (1)H MRS investigation. Am J Transl Res 7:2795–2804

    PubMed  PubMed Central  Google Scholar 

  • Liu T, Li J, Zhao Z, Zhong Y, Zhang Z, Xu Q, Yang G, Lu G, Pan S, Chen F (2016a) Betel quid dependence is associated with functional connectivity changes of the anterior cingulate cortex: a resting-state fMRI study. J Transl Med 14:1

    Article  Google Scholar 

  • Liu T, Li J-j, Zhao Z-y, Yang G-s, Pan M-j, Li C-q, Pan S-y, Chen F (2016b) Altered spontaneous brain activity in betel quid dependence: a resting-state functional magnetic resonance imaging study. Medicine 95.

  • Lo CY, He Y, Lin CP (2011) Graph theoretical analysis of human brain structural networks. Rev Neurosci 22:551–563

    Article  PubMed  Google Scholar 

  • McClernon FJ, Kozink RV, Lutz AM, Rose JE (2009) 24-h smoking abstinence potentiates fMRI-BOLD activation to smoking cues in cerebral cortex and dorsal striatum. Psychopharmacology 204:25–35

    Article  CAS  PubMed  Google Scholar 

  • MHW (2008) 905 betel nut chewing

  • Moerel M, De Martino F, Formisano E (2014) An anatomical and functional topography of human auditory cortical areas. Front Neurosci 8:225

    Article  PubMed  PubMed Central  Google Scholar 

  • Naqvi NH, Rudrauf D, Damasio H, Bechara A (2007) Damage to the insula disrupts addiction to cigarette smoking. Science 315:531–534

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Noël X, Brevers D, Bechara A (2013) A neurocognitive approach to understanding the neurobiology of addiction. Current opinion in neurobiology.

  • Ota M, Noda T, Sato N, Hattori K, Hori H, Sasayama D, Teraishi T, Nagashima A, Obu S, Higuchi T, Kunugi H (2014) White matter abnormalities in major depressive disorder with melancholic and atypical features: a diffusion tensor imaging study. Psychiatry and clinical neurosciences.

  • Robinson TE, Berridge KC (2003) Addiction. Annu Rev Psychol 54:25–53

    Article  PubMed  Google Scholar 

  • Rose JE, McClernon FJ, Froeliger B, Behm FM, Preud’homme X, Krystal AD (2011) Repetitive transcranial magnetic stimulation of the superior frontal gyrus modulates craving for cigarettes. Biol Psychiatry 70:794–799

    Article  PubMed  Google Scholar 

  • Salamone JD, Correa M, Farrar A, Mingote SM (2007) Effort-related functions of nucleus accumbens dopamine and associated forebrain circuits. Psychopharmacology 191:461–482

    Article  CAS  PubMed  Google Scholar 

  • Saunders JB, Aasland OG, Babor TF, Grant M (1993) Development of the Alcohol Use Disorders Identification Test (AUDIT): WHO collaborative project on early detection of persons with harmful alcohol consumption-II. Addiction 88:791–804

    Article  CAS  PubMed  Google Scholar 

  • Shen CY, Tyan YS, Kuo LW, Wu CW, Weng JC (2015) Quantitative evaluation of rabbit brain injury after cerebral hemisphere radiation exposure using generalized q-sampling imaging. PLoS One 10:e0133001

    Article  PubMed  PubMed Central  Google Scholar 

  • Srivastava S, Bhatia MS, Bhargava SK, Kumari R, Chandra S (2015) A diffusion tensor imaging study using a voxel-based analysis, region-of-interest method to analyze white matter abnormalities in first-episode, treatment-naive major depressive disorder. The Journal of neuropsychiatry and clinical neurosciences: appineuropsych15050120.

  • Thomason ME, Thompson PM (2011) Diffusion imaging, white matter, and psychopathology. Annu Rev Clin Psychol 7:63–85

    Article  PubMed  Google Scholar 

  • Tuch DS (2004) Q-ball imaging. Magn Reson Med 52:1358–1372

    Article  PubMed  Google Scholar 

  • Verdejo-Garcia A, Clark L, Dunn BD (2012) The role of interoception in addiction: a critical review. Neuroscience & Biobehavioral Reviews.

  • Volkow ND, Wang G-J, Fowler JS, Tomasi D (2012) Addiction circuitry in the human brain. Annu Rev Pharmacol Toxicol 52:321

    Article  CAS  PubMed  Google Scholar 

  • Walton ME, Behrens TE, Buckley MJ, Rudebeck PH, Rushworth MF (2010) Separable learning systems in the macaque brain and the role of orbitofrontal cortex in contingent learning. Neuron 65:927–939

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Wang Q, Haldar JP, Yeh FC, Xie M, Sun P, Tu TW, Trinkaus K, Klein RS, Cross AH, Song SK (2011) Quantification of increased cellularity during inflammatory demyelination. Brain : a journal of neurology 134:3590–3601

    Article  Google Scholar 

  • Wang X, Cusick MF, Wang Y, Sun P, Libbey JE, Trinkaus K, Fujinami RS, Song SK (2014) Diffusion basis spectrum imaging detects and distinguishes coexisting subclinical inflammation, demyelination and axonal injury in experimental autoimmune encephalomyelitis mice. NMR Biomed 27:843–852

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Watts DJ, Strogatz SH (1998) Collective dynamics of “small-world” networks. Nature 393:440–442

    Article  CAS  PubMed  Google Scholar 

  • Wedeen VJ, Hagmann P, Tseng WY, Reese TG, Weisskoff RM (2005) Mapping complex tissue architecture with diffusion spectrum magnetic resonance imaging. Magn Reson Med 54:1377–1386

    Article  PubMed  Google Scholar 

  • Winstock AR (2002) Areca nut-abuse liability, dependence and public health. Addict Biol 7:133–138

    Article  CAS  PubMed  Google Scholar 

  • Winstock AR, Trivedy CR, Warnakulasuriya KA, Peters TJ (2000) A dependency syndrome related to areca nut use: some medical and psychological aspects among areca nut users in the Gujarat community in the UK. Addict Biol 5:173–179

    Article  CAS  PubMed  Google Scholar 

  • Wise T, Radua J, Nortje G, Cleare AJ, Young AH, Arnone D (2015) Voxel-based meta-analytical evidence of structural disconnectivity in major depression and bipolar disorder. Biological psychiatry.

  • Yeh FC, Wedeen VJ, Tseng WY (2010) Generalized q-sampling imaging. IEEE Trans Med Imaging 29:1626–1635

    Article  PubMed  Google Scholar 

  • Zhang J, Wang J, Wu Q, Kuang W, Huang X, He Y, Gong Q (2011) Disrupted brain connectivity networks in drug-naive, first-episode major depressive disorder. Biol Psychiatry 70:334–342

    Article  PubMed  Google Scholar 

  • Zhang H, Schneider T, Wheeler-Kingshott CA, Alexander DC (2012) NODDI: practical in vivo neurite orientation dispersion and density imaging of the human brain. NeuroImage 61:1000–1016

    Article  PubMed  Google Scholar 

  • Zhang H, Wang Y, Lu T, Qiu B, Tang Y, Ou S, Tie X, Sun C, Xu K (2013) Differences between generalized q-sampling imaging and diffusion tensor imaging in the preoperative visualization of the nerve fiber tracts within peritumoral edema in brain. Neurosurgery 73:1044–1053 discussion 1053

    Article  PubMed  Google Scholar 

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Acknowledgements

The authors appreciate the full support from the Department of Medical Imaging, Chung Shan Medical University Hospital, Taichung, Taiwan. The authors would like to thank Jau-Yang Lin for his assistance in experimental preparation.

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Authors and Affiliations

  1. Department of Medical Imaging and Radiological Sciences, Chung Shan Medical University, Taichung, Taiwan

    Jun-Cheng Weng, Te-Wei Kao & Yeu-Sheng Tyan

  2. Department of Medical Imaging, Chung Shan Medical University Hospital, Taichung, Taiwan

    Jun-Cheng Weng & Yeu-Sheng Tyan

  3. Department of Psychology, Chung Shan Medical University, No.110, Sec. 1, Chien-Kuo N. Road, Taichung, 402, Taiwan

    Guo-Joe Huang & Ming-Chou Ho

  4. Department of Radiation Oncology, Chung Shan Medical University Hospital, Taichung, Taiwan

    Hsien-Chun Tseng

  5. Clinical Psychological Room, Chung Shan Medical University Hospital, Taichung, Taiwan

    Ming-Chou Ho

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  1. Jun-Cheng Weng
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Corresponding author

Correspondence to Ming-Chou Ho.

Ethics declarations

Informed consent was obtained from all participants; the study was approved by the Institutional Review Board of Chung Shan Medical University Hospital. All participants underwent assessment established by psychologists at Chung Shan Medical University, Taichung, Taiwan.

Funding

This study was supported by the research programs NSC103-2420-H-040-001-MY2 and MOST105-2410-H-040-001-MY3, which were sponsored by the Ministry of Science and Technology, Taipei, Taiwan.

Conflict of interest

The authors declare that they have no conflict of interest.

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Appendix

Appendix

The BNDS consists of the following three factors: craving and desire (e.g., if possible, I may chew BQ right now), withdrawal response (e.g., when BQ is not available, I feel so upset that my work and activities are disturbed), and tasting habits (e.g., I care about types, textures, and the feeling that comes from chewing BQ).The eigenvalues of the three factors accounted for 63.10% of total variances, and α coefficients of reliability were between 0.73 to 0.89. Most of model-fit indexes showed good fitting results (RMSEA = 0.070, SRMR = 0.038, AGFI = 0.90, GFI = 0.94, NFI = 0.97, NNFI = 0.98, CFI = 0.98, IFI = 0.98, RFI = 0.96), suggesting optimal construct validity of the scale. The scale also offered criterion-related validity for reference. For example, the BNDS score correlated positively to the number of days per week on which chewing occurred and the average number of BQ chewed per day. The BNDS score correlated negatively to the extent of willing to quit chewing BQ.

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Weng, JC., Kao, TW., Huang, GJ. et al. Evaluation of structural connectivity changes in betel-quid chewers using generalized q-sampling MRI. Psychopharmacology 234, 1945–1955 (2017). https://doi.org/10.1007/s00213-017-4602-0

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