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Associations of alcohol use, HIV infection, and age with brain white matter microstructure

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Abstract

Heavy drinking and HIV infection are independently associated with damage to the brain’s white matter. The purpose of the current study was to investigate whether current alcohol consumption, HIV infection, and associated characteristics were associated with indices of white matter microstructural integrity in people living with HIV (PLWH) and seronegative individuals. PLWH and controls were categorized as non-drinkers, moderate drinkers, or heavy drinkers. White matter fractional anisotropy (FA), radial diffusivity (RD), and axial diffusivity (AD) were assessed using diffusion tensor imaging (DTI). Voxelwise analyses using tract-based spatial statistics were followed by confirmatory region-of-interest (ROI) analyses. Data from 108 participants (62 PLWH, 46 controls) were suitable for analysis. Average age (± standard deviation) was 45.2 ± 11.1 years, and the sample was 42% female. The majority of PLWH were on antiretroviral therapy (94%) and were virally suppressed (69%). PLWH and controls did not differ on substance use. Heavier alcohol intake was significantly associated with lower FA and higher RD in widespread areas. Heavy drinking was significantly associated with higher AD in a small region. The main effect of HIV was not significant, but a significant HIV-age interaction was observed. Follow-up ROI analyses confirmed the main effect of drinking group and HIV-age interaction. In conclusion, results are consistent with a dose-dependent association of alcohol use with lower white matter microstructural coherence. Concordance between FA and RD findings suggests dysmyelination as a mechanism. Findings underscore the need to address unhealthy alcohol use in HIV-positive and seronegative individuals, the consequences of which may be exacerbated by aging.

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References

  • Alhassoon OM, Sorg SF, Taylor MJ, Stephan RA, Schweinsburg BC, Stricker NH, Gongvatana A, Grant I (2012) Callosal white matter microstructural recovery in abstinent alcoholics: a longitudinal diffusion tensor imaging study. Alcohol Clin Exp Res 36:1922–1931

    Article  PubMed  PubMed Central  Google Scholar 

  • Amen DG, Egan S, Meysami S, Raji CA, George N (2018) Patterns of regional cerebral blood flow as a function of age throughout the lifespan. J Alzheimers Dis 65:1087–1092

    Article  CAS  PubMed  Google Scholar 

  • Avants BB, Tustison NJ, Song G, Cook PA, Klein A, Gee JC (2011) A reproducible evaluation of ANTs similarity metric performance in brain image registration. Neuroimage 54:2033–2044

    Article  PubMed  Google Scholar 

  • Basser PJ, Pierpaoli C (1996) Microstructural and physiological features of tissues elucidated by quantitative-diffusion-tensor MRI. J Magn Reson B 111:209–219

    Article  CAS  PubMed  Google Scholar 

  • Borghesani PR, Madhyastha TM, Aylward EH, Reiter MA, Swarny BR, Schaie KW, Willis SL (2013) The association between higher order abilities, processing speed, and age are variably mediated by white matter integrity during typical aging. Neuropsychologia 51:1435–1444

    Article  PubMed  Google Scholar 

  • Centers for Disease Control and Prevention (2019) Behavioral and clinical characteristics of persons with diagnosed HIV infection. Medical Monitoring Project, United States, 2017 Cycle (June 2017-May 2018)

  • Coelho A, Fernandes HM, Magalhães R, Moreira PS, Marques P, Soares JM, Amorim L, Portugal-Nunes C, Castanho T, Santos NC, Sousa N (2021) Signatures of white-matter microstructure degradation during aging and its association with cognitive status. Sci Rep 11:4517

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cohen RA, Gullett JM, Porges EC, Woods AJ, Lamb DG, Bryant VE, McAdams M, Tashima K, Cook R, Bryant K, Monnig M, Kahler CW, Monti PM (2019) Heavy alcohol use and age effects on HIV-associated neurocognitive function. Alcohol Clin Exp Res 43:147–157

    CAS  PubMed  Google Scholar 

  • Cohen RA, Harezlak J, Schifitto G, Hana G, Clark U, Gongvatana A, Paul R, Taylor M, Thompson P, Alger J, Brown M, Zhong J, Campbell T, Singer E, Daar E, McMahon D, Tso Y, Yiannoutsos CT, Navia B (2010) Effects of nadir CD4 count and duration of human immunodeficiency virus infection on brain volumes in the highly active antiretroviral therapy era. J Neurovirol 16:25–32

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole JH, Caan MWA, Underwood J, De Francesco D, van Zoest RA, Wit FWNM, Mutsaerts HJMM, Leech R, Geurtsen GJ, Portegies P, Majoie CBLM, Schim van der Loeff MF, Sabin CA, Reiss P, Winston A, Sharp DJ, CiRtAC C (2018) No evidence for accelerated aging-related brain pathology in treated human immunodeficiency virus: Longitudinal Neuroimaging Results From the Comorbidity in Relation to AIDS (COBRA) Project. Clin Infect Dis 66:1899–1909

    Article  PubMed  Google Scholar 

  • Coupe P, Yger P, Prima S, Hellier P, Kervrann C, Barillot C (2008) An optimized blockwise nonlocal means denoising filter for 3-D magnetic resonance images. IEEE Trans Med Imaging 27:425–441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Crespi C, Galandra C, Canessa N, Manera M, Poggi P, Basso G (2020) Microstructural damage of white-matter tracts connecting large-scale networks is related to impaired executive profile in alcohol use disorder. Neuroimage Clin 25:102141

  • Crews FT (2008) Alcohol-related neurodegeneration and recovery: mechanisms from animal models. Alcohol Res Health 31:377–388

    PubMed  PubMed Central  Google Scholar 

  • Cysique LA, Soares JR, Geng G, Scarpetta M, Moffat K, Green M, Brew BJ, Henry RG, Rae C (2017) White matter measures are near normal in controlled HIV infection except in those with cognitive impairment and longer HIV duration. J Neurovirol 23:539–547

    Article  PubMed  Google Scholar 

  • Fennema-Notestine C, Ellis RJ, Archibald SL, Jernigan TL, Letendre SL, Notestine RJ, Taylor MJ, Theilmann RJ, Julaton MD, Croteau DJ, Wolfson T, Heaton RK, Gamst AC, Franklin DR Jr, Clifford DB, Collier AC, Gelman BB, Marra C, McArthur JC, McCutchan JA, Morgello S, Simpson DM, Grant I (2013) Increases in brain white matter abnormalities and subcortical gray matter are linked to CD4 recovery in HIV infection. J Neurovirol 19:393–401

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Filbey FM, Aslan S, Calhoun VD, Spence JS, Damaraju E, Caprihan A, Segall J (2014) Long-term effects of marijuana use on the brain. Proc Natl Acad Sci U S A 111:16913–16918

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischl B (2012) FreeSurfer Neuroimage 62:774–781

    Article  PubMed  Google Scholar 

  • Fischl B, Salat DH, Busa E, Albert M, Dieterich M, Haselgrove C, van der Kouwe A, Killiany R, Kennedy D, Klaveness S, Montillo A, Makris N, Rosen B, Dale AM (2002) Whole brain segmentation: automated labeling of neuroanatomical structures in the human brain. Neuron 33:341–355

    Article  CAS  PubMed  Google Scholar 

  • Gongvatana A, Cohen RA, Correia S, Devlin KN, Miles J, Kang H, Ombao H, Navia B, Laidlaw DH, Tashima KT (2011) Clinical contributors to cerebral white matter integrity in HIV-infected individuals. J Neurovirol 17:477–486

    Article  PubMed  PubMed Central  Google Scholar 

  • Gongvatana A, Schweinsburg BC, Taylor MJ, Theilmann RJ, Letendre SL, Alhassoon OM, Jacobus J, Woods SP, Jernigan TL, Ellis RJ, Frank LR, Grant I (2009) White matter tract injury and cognitive impairment in human immunodeficiency virus-infected individuals. J Neurovirol 15:187–195

    Article  PubMed  PubMed Central  Google Scholar 

  • Gullett JM, Lamb DG, Porges E, Woods AJ, Rieke J, Thompson P, Jahanshad N, Nir TM, Tashima K, Cohen RA (2018) The impact of alcohol use on frontal white matter in HIV. Alcohol Clin Exp Res 42:1640–1649

    Article  PubMed  PubMed Central  Google Scholar 

  • Heaps-Woodruff JM, Wright PW, Ances BM, Clifford D, Paul RH (2016) The impact of human immune deficiency virus and hepatitis C coinfection on white matter microstructural integrity. J Neurovirol 22:389–399

    Article  CAS  PubMed  Google Scholar 

  • Heaton RK, Clifford DB, Franklin DR, Woods SP, Ake C, Vaida F, Ellis RJ, Letendre SL, Marcotte TD, Atkinson JH, Rivera-Mindt M, Vigil OR, Taylor MJ, Collier AC, Marra CM, Gelman BB, McArthur JC, Morgello S, Simpson DM, McCutchan JA, Abramson I, Gamst A, Fennema-Notestine C, Jernigan TL, Wong J, Grant I, CG, (2010) HIV-associated neurocognitive disorders persist in the era of potent antiretroviral therapy: CHARTER Study. Neurology 75:2087–2096

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Inano S, Takao H, Hayashi N, Abe O, Ohtomo K (2011) Effects of age and gender on white matter integrity. AJNR Am J Neuroradiol 32:2103–2109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jenkinson M, Beckmann CF, Behrens TE, Woolrich MW, Smith SM (2012) FSL Neuroimage 62:782–790

    Article  PubMed  Google Scholar 

  • Kievit RA, Davis SW, Mitchell DJ, Taylor JR, Duncan J, Henson RN (2014) Distinct aspects of frontal lobe structure mediate age-related differences in fluid intelligence and multitasking. Nat Commun 5:5658

    Article  CAS  PubMed  Google Scholar 

  • Kuhn T, Jin Y, Huang C, Kim Y, Nir TM, Gullett JM, Jones JD, Sayegh P, Chung C, Dang BH, Singer EJ, Shattuck DW, Jahanshad N, Bookheimer SY, Hinkin CH, Zhu H, Thompson PM, Thames AD (2019) The joint effect of aging and HIV infection on microstructure of white matter bundles. Hum Brain Mapp 40:4370–4380

    Article  PubMed  PubMed Central  Google Scholar 

  • Kuhn T, Kaufmann T, Doan NT, Westlye LT, Jones J, Nunez RA, Bookheimer SY, Singer EJ, Hinkin CH, Thames AD (2018) An augmented aging process in brain white matter in HIV. Hum Brain Mapp 39:2532–2540

    Article  PubMed  PubMed Central  Google Scholar 

  • Liang H, Chang L, Chen R, Oishi K, Ernst T (2018) Independent and combined effects of chronic HIV-infection and tobacco smoking on brain microstructure. J Neuroimmune Pharmacol 13:509–522

    Article  PubMed  PubMed Central  Google Scholar 

  • Madden DJ, Spaniol J, Costello MC, Bucur B, White LE, Cabeza R, Davis SW, Dennis NA, Provenzale JM, Huettel SA (2009) Cerebral white matter integrity mediates adult age differences in cognitive performance. J Cogn Neurosci 21:289–302

    Article  PubMed  PubMed Central  Google Scholar 

  • Manjón JV, Coupé P, Concha L, Buades A, Collins DL, Robles M (2013).Diffusion weighted image denoising using overcomplete local PCA. PLoS One 8:e73021

  • Monnig MA (2016) Immune activation and neuroinflammation in alcohol use and HIV infection: evidence for shared mechanisms. Am J Drug Alcohol Abuse 1–17

  • Monnig MA, Caprihan A, Yeo RA, Gasparovic C, Ruhl DA, Lysne P, Bogenschutz MP, Hutchison KE, Thoma RJ (2013a) Diffusion tensor imaging of white matter networks in individuals with current and remitted alcohol use disorders and comorbid conditions. Psychol Addict Behav 27:455–65. PMCID: PMC3374918

  • Monnig MA, Tonigan JS, Yeo RA, Thoma RJ, McCrady BS (2013b) White matter volume in alcohol use disorders: a meta-analysis. Addict Biol 18:581–92; PMCID: PMC3390447

  • Mori S, Oishi K, Jiang H, Jiang L, Li X, Akhter K, Hua K, Faria AV, Mahmood A, Woods R, Toga AW, Pike GB, Neto PR, Evans A, Zhang J, Huang H, Miller MI, van Zijl P, Mazziotta J (2008) Stereotaxic white matter atlas based on diffusion tensor imaging in an ICBM template. Neuroimage 40:570–582

    Article  PubMed  Google Scholar 

  • National Institute on Alcohol Abuse and Alcoholism (2010) Rethinking drinking: alcohol and your health. Services USDoHaH, (ed): Bethesda, MD

  • Nir TM, Jahanshad N, Busovaca E, Wendelken L, Nicolas K, Thompson PM, Valcour VG (2014) Mapping white matter integrity in elderly people with HIV. Hum Brain Mapp 35:975–992

    Article  PubMed  Google Scholar 

  • O’Connor EE, Jaillard A, Renard F, Zeffiro TA (2017) Reliability of white matter microstructural changes in HIV infection: meta-analysis and confirmation. AJNR Am J Neuroradiol 38:1510–1519

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • O’Connor EE, Zeffiro TA (2018) Brain structural changes following HIV infection: meta-analysis. AJNR Am J Neuroradiol 39:54–62

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Orr JM, Paschall CJ, Banich MT (2016) Recreational marijuana use impacts white matter integrity and subcortical (but not cortical) morphometry. Neuroimage Clin 12:47–56

    Article  PubMed  PubMed Central  Google Scholar 

  • Penke L, Maniega SM, Bastin ME, Valdés Hernández MC, Murray C, Royle NA, Starr JM, Wardlaw JM, Deary IJ (2012) Brain white matter tract integrity as a neural foundation for general intelligence. Mol Psychiatry 17:1026–1030

    Article  CAS  PubMed  Google Scholar 

  • Penke L, Muñoz Maniega S, Murray C, Gow AJ, Hernández MC, Clayden JD, Starr JM, Wardlaw JM, Bastin ME, Deary IJ (2010) A general factor of brain white matter integrity predicts information processing speed in healthy older people. J Neurosci 30:7569–7574

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pfefferbaum A, Adalsteinsson E, Sullivan EV (2006) Supratentorial profile of white matter microstructural integrity in recovering alcoholic men and women. Biol Psychiatry 59:364–372

    Article  PubMed  Google Scholar 

  • Pfefferbaum A, Rosenbloom M, Rohlfing T, Sullivan EV (2009) Degradation of association and projection white matter systems in alcoholism detected with quantitative fiber tracking. Biol Psychiatry 65:680–690

    Article  CAS  PubMed  Google Scholar 

  • Pfefferbaum A, Rosenbloom MJ, Adalsteinsson E, Sullivan EV (2007) Diffusion tensor imaging with quantitative fibre tracking in HIV infection and alcoholism comorbidity: synergistic white matter damage. Brain 130:48–64

    Article  PubMed  Google Scholar 

  • Pfefferbaum A, Rosenbloom MJ, Chu W, Sassoon SA, Rohlfing T, Pohl KM, Zahr NM, Sullivan EV (2014) White matter microstructural recovery with abstinence and decline with relapse in alcohol dependence interacts with normal ageing: a controlled longitudinal DTI study. Lancet Psychiatry 1:202–212

    Article  PubMed  PubMed Central  Google Scholar 

  • Ragin AB, Wu Y, Gao Y, Keating S, Du H, Sammet C, Kettering CS, Epstein LG (2015) Brain alterations within the first 100 days of HIV infection. Ann Clin Transl Neurol 2:12–21

    Article  PubMed  Google Scholar 

  • Rubin LH, Maki PM (2019) HIV, depression, and cognitive impairment in the era of effective antiretroviral therapy. Curr HIV/AIDS Rep 16:82–95

    Article  PubMed  PubMed Central  Google Scholar 

  • Schulte T, Müller-Oehring EM, Sullivan EV, Pfefferbaum A (2012) White matter fiber compromise contributes differentially to attention and emotion processing impairment in alcoholism, HIV-infection, and their comorbidity. Neuropsychologia 50:2812–2822

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Seider TR, Gongvatana A, Woods AJ, Chen H, Porges EC, Cummings T, Correia S, Tashima K, Cohen RA (2016) Age exacerbates HIV-associated white matter abnormalities. J Neurovirol 22:201–212

    Article  PubMed  Google Scholar 

  • Sexton CE, Walhovd KB, Storsve AB, Tamnes CK, Westlye LT, Johansen-Berg H, Fjell AM (2014) Accelerated changes in white matter microstructure during aging: a longitudinal diffusion tensor imaging study. J Neurosci 34:15425–15436

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sheehan DV, Lecrubier Y, Sheehan KH, Amorim P, Janavs J, Weiller E, Hergueta T, Baker R, Dunbar GC (1998) The Mini-International Neuropsychiatric Interview (M.I.N.I.): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59 Suppl 20:22–33;quiz 34–57

  • Sled JG, Zijdenbos AP, Evans AC (1998) A nonparametric method for automatic correction of intensity nonuniformity in MRI data. IEEE Trans Med Imaging 17:87–97

    Article  CAS  PubMed  Google Scholar 

  • Smith SM, Jenkinson M, Johansen-Berg H, Rueckert D, Nichols TE, Mackay CE, Watkins KE, Ciccarelli O, Cader MZ, Matthews PM, Behrens TE (2006) Tract-based spatial statistics: voxelwise analysis of multi-subject diffusion data. Neuroimage 31:1487–1505

    Article  PubMed  Google Scholar 

  • Sobell LC, Sobell MB (1992). In: Allen J, Litten RZ (eds) Measuring alcohol consumption: psychosocial and biological methods. Humana Press, Totowa, NJ, pp 41–72

    Chapter  Google Scholar 

  • Song SK, Sun SW, Ramsbottom MJ, Chang C, Russell J, Cross AH (2002) Dysmyelination revealed through MRI as increased radial (but unchanged axial) diffusion of water. Neuroimage 17:1429–1436

    Article  PubMed  Google Scholar 

  • Song SK, Yoshino J, Le TQ, Lin SJ, Sun SW, Cross AH, Armstrong RC (2005) Demyelination increases radial diffusivity in corpus callosum of mouse brain. Neuroimage 26:132–140

    Article  PubMed  Google Scholar 

  • Su T, Caan MW, Wit FW, Schouten J, Geurtsen GJ, Cole JH, Sharp DJ, Vos FM, Prins M, Portegies P, Reiss P, Majoie CB (2016) White matter structure alterations in HIV-1-infected men with sustained suppression of viraemia on treatment. AIDS 30:311–322

    Article  CAS  PubMed  Google Scholar 

  • Sullivan EV, Harris RA, Pfefferbaum A (2010) Alcohol’s effects on brain and behavior. Alcohol Res Health 33:127–143

    PubMed  PubMed Central  Google Scholar 

  • Trivedi R, Bagga D, Bhattacharya D, Kaur P, Kumar P, Khushu S, Tripathi RP, Singh N (2013) White matter damage is associated with memory decline in chronic alcoholics: a quantitative diffusion tensor tractography study. Behav Brain Res 250:192–198

    Article  CAS  PubMed  Google Scholar 

  • Vernooij MW, Ikram MA, Vrooman HA, Wielopolski PA, Krestin GP, Hofman A, Niessen WJ, Van der Lugt A, Breteler MM (2009) White matter microstructural integrity and cognitive function in a general elderly population. Arch Gen Psychiatry 66:545–553

    Article  PubMed  Google Scholar 

  • Vinke EJ, de Groot M, Venkatraghavan V, Klein S, Niessen WJ, Ikram MA, Vernooij MW (2018) Trajectories of imaging markers in brain aging: the Rotterdam Study. Neurobiol Aging 71:32–40

    Article  PubMed  Google Scholar 

  • Williams EC, Hahn JA, Saitz R, Bryant K, Lira MC, Samet JH (2016) Alcohol use and human immunodeficiency virus (HIV) infection: current knowledge, implications, and future directions. Alcohol Clin Exp Res 40:2056–2072

    Article  PubMed  PubMed Central  Google Scholar 

  • Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397

    Article  PubMed  Google Scholar 

  • Yeh PH, Simpson K, Durazzo TC, Gazdzinski S, Meyerhoff DJ (2009) Tract-Based Spatial Statistics (TBSS) of diffusion tensor imaging data in alcohol dependence: abnormalities of the motivational neurocircuitry. Psychiatry Res 173:22–30

    Article  PubMed  PubMed Central  Google Scholar 

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Funding

This research was supported by National Institute on Alcohol Abuse and Alcoholism grants K23AA024704 (PI: Monnig), P01AA019072 (PI: Monti), K05AA019681 (PI: Monti), U01-AA020797-09 (Co-I: Gullett), and K01AA025306 (PI: Porges); by National Institute of Biomedical Imaging and Bioengineering grants U54EB020403 (PI: Thompson) and P41EB015922 (PI: Thompson); by National Institute on Aging grants R01AG059874 (PI: Jahanshad) and T32AG058507 (PI: Toga); by National Institute of General Medical Sciences grant P20GM130414 (PI: Monti); and by the National Institute of Allergy and Infectious Diseases grant to the Providence/Boston Center for AIDS Research (P30AI042853). Coauthors NJ, PT, and TN also received partial grant support from Biogen, Inc., for research unrelated to this work. Study sponsors had no role in study design; in the collection, analysis and interpretation of data; in the writing of the report; or in the decision to submit the article for publication.

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Authors and Affiliations

  1. Brown University, Box G-S121-5, Providence, RI, 02912, USA

    Mollie A. Monnig & Peter M. Monti

  2. Department of Clinical and Health Psychology, University of Florida, Gainesville, FL, 32611, USA

    Joseph M. Gullett, Eric C. Porges, Adam J. Woods & Ronald A. Cohen

  3. The Miriam Hospital, Providence, RI, 02903, USA

    Karen Tashima

  4. Keck School of Medicine, University of Southern California, Los Angeles, CA, 90033, USA

    Neda Jahanshad, Paul Thompson & Talia Nir

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  1. Mollie A. Monnig
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  2. Joseph M. Gullett
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  10. Ronald A. Cohen
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Contributions

RAC and PMM conceptualized and obtained funding for the study. NJ, PT, and TN provided resources in the form of DTI analysis tools. AJW, ECP, JMG, and MAM performed project administration and data curation. MAM conducted formal analysis and wrote the original draft. All coauthors reviewed and edited the manuscript.

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Correspondence to Mollie A. Monnig.

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Monnig, M.A., Gullett, J.M., Porges, E.C. et al. Associations of alcohol use, HIV infection, and age with brain white matter microstructure. J. Neurovirol. 27, 936–950 (2021). https://doi.org/10.1007/s13365-021-01021-8

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