Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort

Leonardo Tozzi; Lisa Garczarek; Deborah Janowitz; Dan J. Stein; Katharina Wittfeld; Henrik Dobrowolny; Jim Lagopoulos; Sean N. Hatton; Ian B. Hickie; Angela Carballedo; Samantha J. Brooks; Daniella Vuletic; Anne Uhlmann; Ilya M. Veer; Henrik Walter; Robin Bülow; Henry Völzke; Johanna Klinger-König; Knut Schnell; Dieter Schoepf; Dominik Grotegerd; Nils Opel; Udo Dannlowski; Harald Kugel; Elisabeth Schramm; Carsten Konrad; Tilo Kircher; Dilara Jüksel; Igor Nenadić; Axel Krug; Tim Hahn; Olaf Steinsträter; Ronny Redlich; Dario Zaremba; Bartosz Zurowski; Cynthia H.Y. Fu; Danai Dima; James Cole; Hans J. Grabe; Colm G. Connolly; Tony T. Yang; Tiffany C. Ho; Kaja Z. Lewinn; Meng Li; Nynke A. Groenewold; Lauren E. Salminen; Martin Walter; Alan N. Simmons; Theo G.M. Van Erp; Neda Jahanshad; Bernhard T. Baune; Nic J.A. Van Der Wee; Marie Jose Van Tol; Brenda W.J.H. Penninx; Derrek P. Hibar; Paul M. Thompson; Dick J. Veltman; Lianne Schmaal; Thomas Frodl

doi:10.1017/S003329171900093X

Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort

Leonardo Tozzi, Lisa Garczarek, Deborah Janowitz, Dan J. Stein, Katharina Wittfeld, Henrik Dobrowolny, Jim Lagopoulos, Sean N. Hatton, Ian B. Hickie, Angela Carballedo, Samantha J. Brooks, Daniella Vuletic, Anne Uhlmann, Ilya M. Veer, Henrik Walter, Robin Bülow, Henry Völzke, Johanna Klinger-König, Knut Schnell, Dieter SchoepfDominik Grotegerd, Nils Opel, Udo Dannlowski, Harald Kugel, Elisabeth Schramm, Carsten Konrad, Tilo Kircher, Dilara Jüksel, Igor Nenadić, Axel Krug, Tim Hahn, Olaf Steinsträter, Ronny Redlich, Dario Zaremba, Bartosz Zurowski, Cynthia H.Y. Fu, Danai Dima, James Cole, Hans J. Grabe, Colm G. Connolly, Tony T. Yang, Tiffany C. Ho, Kaja Z. Lewinn, Meng Li, Nynke A. Groenewold, Lauren E. Salminen, Martin Walter, Alan N. Simmons, Theo G.M. Van Erp, Neda Jahanshad, Bernhard T. Baune, Nic J.A. Van Der Wee, Marie Jose Van Tol, Brenda W.J.H. Penninx, Derrek P. Hibar, Paul M. Thompson, Dick J. Veltman, Lianne Schmaal, Thomas Frodl

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68 Citations (Scopus)

Résumé

Background Childhood maltreatment (CM) plays an important role in the development of major depressive disorder (MDD). The aim of this study was to examine whether CM severity and type are associated with MDD-related brain alterations, and how they interact with sex and age.Methods Within the ENIGMA-MDD network, severity and subtypes of CM using the Childhood Trauma Questionnaire were assessed and structural magnetic resonance imaging data from patients with MDD and healthy controls were analyzed in a mega-analysis comprising a total of 3872 participants aged between 13 and 89 years. Cortical thickness and surface area were extracted at each site using FreeSurfer.Results CM severity was associated with reduced cortical thickness in the banks of the superior temporal sulcus and supramarginal gyrus as well as with reduced surface area of the middle temporal lobe. Participants reporting both childhood neglect and abuse had a lower cortical thickness in the inferior parietal lobe, middle temporal lobe, and precuneus compared to participants not exposed to CM. In males only, regardless of diagnosis, CM severity was associated with higher cortical thickness of the rostral anterior cingulate cortex. Finally, a significant interaction between CM and age in predicting thickness was seen across several prefrontal, temporal, and temporo-parietal regions.Conclusions Severity and type of CM may impact cortical thickness and surface area. Importantly, CM may influence age-dependent brain maturation, particularly in regions related to the default mode network, perception, and theory of mind.

Langue d'origine	English
Pages (de-à)	1020-1031
Nombre de pages	12
Journal	Psychological Medicine
Volume	50
Numéro de publication	6
DOI	https://doi.org/10.1017/S003329171900093X
Statut de publication	Published - avr. 1 2020
Publié à l'externe	Oui

Note bibliographique

Funding Information:
group gratefully acknowledges support from the NIH BD2 K award, U54 EB020403. The infrastructure for the NESDA study (http://www.nesda.nl) is funded through the Geestkracht program of the Netherlands Organisation for Health Research and Development (Zon-Mw, grant number 10-000-1002) and is supported by participating universities (VU University Medical Center, GGZ inGeest, Arkin, Leiden University Medical Center, GGZ Rivierduinen, University Medical Center Groningen) and mental health care organizations, see http://www.nesda.nl. Lianne Schmaal is supported by The Netherlands Brain Foundation Grant number F2014(1)-24 and the Neuroscience Campus Amsterdam Scientific Excellence grant (IPB-SE-15-PSYCH-Schmaal).

Funding Information:
Financial support. The Münster Neuroimaging Cohort was funded by the German Research Foundation (SFB-TRR58, Projects C09 and Z02 to UD) and the Interdisciplinary Center for Clinical Research (IZKF) of the medical faculty of Münster (grant Dan3/012/17 to UD). FOR2107-Marburg was funded by the German Research Foundation (DFG, grant FOR2107 KI588/ 14-1, KI588/15-1, KI588/14-2, KI588/15-2 to TK, KR3822/5-1 to AK). FOR2107-Münster was funded by the German Research Foundation (DFG, grant FOR2107 HA 7070/2-2 to TH; DA1151/5-1 and DA1151/5-2 to UD).

Funding Information:
ENIGMA was supported in part by a Consortium grant (U54 EB020403 to PMT, DPH, NJ) from the NIH Institutes contributing to the Big Data to Knowledge (BD2 K) Initiative, and by R01 MH116147 and R56 AG058854. Moreover, an NIH BD2 K award, U54EB020403 to T.G.M. van Erp. London: This paper represents independent research [part] funded by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. SHIP: The Study of Health in Pomerania (SHIP) is supported by the German Federal Ministry of Education and Research (grants 01ZZ9603, 01ZZ0103, and 01ZZ0403) the Ministry of Cultural Affairs as well as the Social Ministry of the Federal State of Mecklenburg-West Pomerania. MRI scans were supported by Siemens Healthcare, Erlangen, Germany. SHIP-LEGEND was supported by the German Research Foundation (GR1912/5-1). Dublin: The study was supported by a Science Foundation Ireland (SFI) Stokes Professorship Grant to Thomas Frodl. San Francisco: This work was supported by the Brain and Behavior Research Foundation (formerly NARSAD) to T.T.Y.; the National Institute of Mental Health (R01MH085734 to T.T.Y.; K01MH097978 to K.Z.L.; K01MH117442 to T.C.H.) and by the American Foundation for Suicide Prevention (PDF-1-064-13) to T.C.H.

Publisher Copyright:
Copyright © 2019 Cambridge University Press.

ASJC Scopus Subject Areas

Applied Psychology
Psychiatry and Mental health

ODD de l’ONU

Cette action contribue à la réalisation des objectifs de développement durable suivants

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10.1017/S003329171900093X

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Tozzi, L., Garczarek, L., Janowitz, D., Stein, D. J., Wittfeld, K., Dobrowolny, H., Lagopoulos, J., Hatton, S. N., Hickie, I. B., Carballedo, A., Brooks, S. J., Vuletic, D., Uhlmann, A., Veer, I. M., Walter, H., Bülow, R., Völzke, H., Klinger-König, J., Schnell, K., ... Frodl, T. (2020). Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort. Psychological Medicine, 50(6), 1020-1031. https://doi.org/10.1017/S003329171900093X

Tozzi, L, Garczarek, L, Janowitz, D, Stein, DJ, Wittfeld, K, Dobrowolny, H, Lagopoulos, J, Hatton, SN, Hickie, IB, Carballedo, A, Brooks, SJ, Vuletic, D, Uhlmann, A, Veer, IM, Walter, H, Bülow, R, Völzke, H, Klinger-König, J, Schnell, K, Schoepf, D, Grotegerd, D, Opel, N, Dannlowski, U, Kugel, H, Schramm, E, Konrad, C, Kircher, T, Jüksel, D, Nenadić, I, Krug, A, Hahn, T, Steinsträter, O, Redlich, R, Zaremba, D, Zurowski, B, Fu, CHY, Dima, D, Cole, J, Grabe, HJ, Connolly, CG, Yang, TT, Ho, TC, Lewinn, KZ, Li, M, Groenewold, NA, Salminen, LE, Walter, M, Simmons, AN, Van Erp, TGM, Jahanshad, N, Baune, BT, Van Der Wee, NJA, Van Tol, MJ, Penninx, BWJH, Hibar, DP, Thompson, PM, Veltman, DJ, Schmaal, L & Frodl, T 2020, 'Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort', Psychological Medicine, vol. 50, n° 6, pp. 1020-1031. https://doi.org/10.1017/S003329171900093X

@article{02f108f964dc41528e1d79f49fb7d38b,

title = "Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort",

abstract = "Background Childhood maltreatment (CM) plays an important role in the development of major depressive disorder (MDD). The aim of this study was to examine whether CM severity and type are associated with MDD-related brain alterations, and how they interact with sex and age.Methods Within the ENIGMA-MDD network, severity and subtypes of CM using the Childhood Trauma Questionnaire were assessed and structural magnetic resonance imaging data from patients with MDD and healthy controls were analyzed in a mega-analysis comprising a total of 3872 participants aged between 13 and 89 years. Cortical thickness and surface area were extracted at each site using FreeSurfer.Results CM severity was associated with reduced cortical thickness in the banks of the superior temporal sulcus and supramarginal gyrus as well as with reduced surface area of the middle temporal lobe. Participants reporting both childhood neglect and abuse had a lower cortical thickness in the inferior parietal lobe, middle temporal lobe, and precuneus compared to participants not exposed to CM. In males only, regardless of diagnosis, CM severity was associated with higher cortical thickness of the rostral anterior cingulate cortex. Finally, a significant interaction between CM and age in predicting thickness was seen across several prefrontal, temporal, and temporo-parietal regions.Conclusions Severity and type of CM may impact cortical thickness and surface area. Importantly, CM may influence age-dependent brain maturation, particularly in regions related to the default mode network, perception, and theory of mind.",

author = "Leonardo Tozzi and Lisa Garczarek and Deborah Janowitz and Stein, {Dan J.} and Katharina Wittfeld and Henrik Dobrowolny and Jim Lagopoulos and Hatton, {Sean N.} and Hickie, {Ian B.} and Angela Carballedo and Brooks, {Samantha J.} and Daniella Vuletic and Anne Uhlmann and Veer, {Ilya M.} and Henrik Walter and Robin B{\"u}low and Henry V{\"o}lzke and Johanna Klinger-K{\"o}nig and Knut Schnell and Dieter Schoepf and Dominik Grotegerd and Nils Opel and Udo Dannlowski and Harald Kugel and Elisabeth Schramm and Carsten Konrad and Tilo Kircher and Dilara J{\"u}ksel and Igor Nenadi{\'c} and Axel Krug and Tim Hahn and Olaf Steinstr{\"a}ter and Ronny Redlich and Dario Zaremba and Bartosz Zurowski and Fu, {Cynthia H.Y.} and Danai Dima and James Cole and Grabe, {Hans J.} and Connolly, {Colm G.} and Yang, {Tony T.} and Ho, {Tiffany C.} and Lewinn, {Kaja Z.} and Meng Li and Groenewold, {Nynke A.} and Salminen, {Lauren E.} and Martin Walter and Simmons, {Alan N.} and {Van Erp}, {Theo G.M.} and Neda Jahanshad and Baune, {Bernhard T.} and {Van Der Wee}, {Nic J.A.} and {Van Tol}, {Marie Jose} and Penninx, {Brenda W.J.H.} and Hibar, {Derrek P.} and Thompson, {Paul M.} and Veltman, {Dick J.} and Lianne Schmaal and Thomas Frodl",

note = "Funding Information: group gratefully acknowledges support from the NIH BD2 K award, U54 EB020403. The infrastructure for the NESDA study (http://www.nesda.nl) is funded through the Geestkracht program of the Netherlands Organisation for Health Research and Development (Zon-Mw, grant number 10-000-1002) and is supported by participating universities (VU University Medical Center, GGZ inGeest, Arkin, Leiden University Medical Center, GGZ Rivierduinen, University Medical Center Groningen) and mental health care organizations, see http://www.nesda.nl. Lianne Schmaal is supported by The Netherlands Brain Foundation Grant number F2014(1)-24 and the Neuroscience Campus Amsterdam Scientific Excellence grant (IPB-SE-15-PSYCH-Schmaal). Funding Information: Financial support. The M{\"u}nster Neuroimaging Cohort was funded by the German Research Foundation (SFB-TRR58, Projects C09 and Z02 to UD) and the Interdisciplinary Center for Clinical Research (IZKF) of the medical faculty of M{\"u}nster (grant Dan3/012/17 to UD). FOR2107-Marburg was funded by the German Research Foundation (DFG, grant FOR2107 KI588/ 14-1, KI588/15-1, KI588/14-2, KI588/15-2 to TK, KR3822/5-1 to AK). FOR2107-M{\"u}nster was funded by the German Research Foundation (DFG, grant FOR2107 HA 7070/2-2 to TH; DA1151/5-1 and DA1151/5-2 to UD). Funding Information: ENIGMA was supported in part by a Consortium grant (U54 EB020403 to PMT, DPH, NJ) from the NIH Institutes contributing to the Big Data to Knowledge (BD2 K) Initiative, and by R01 MH116147 and R56 AG058854. Moreover, an NIH BD2 K award, U54EB020403 to T.G.M. van Erp. London: This paper represents independent research [part] funded by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King{\textquoteright}s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. SHIP: The Study of Health in Pomerania (SHIP) is supported by the German Federal Ministry of Education and Research (grants 01ZZ9603, 01ZZ0103, and 01ZZ0403) the Ministry of Cultural Affairs as well as the Social Ministry of the Federal State of Mecklenburg-West Pomerania. MRI scans were supported by Siemens Healthcare, Erlangen, Germany. SHIP-LEGEND was supported by the German Research Foundation (GR1912/5-1). Dublin: The study was supported by a Science Foundation Ireland (SFI) Stokes Professorship Grant to Thomas Frodl. San Francisco: This work was supported by the Brain and Behavior Research Foundation (formerly NARSAD) to T.T.Y.; the National Institute of Mental Health (R01MH085734 to T.T.Y.; K01MH097978 to K.Z.L.; K01MH117442 to T.C.H.) and by the American Foundation for Suicide Prevention (PDF-1-064-13) to T.C.H. Publisher Copyright: Copyright {\textcopyright} 2019 Cambridge University Press.",

year = "2020",

month = apr,

day = "1",

doi = "10.1017/S003329171900093X",

language = "English",

volume = "50",

pages = "1020--1031",

journal = "Psychological Medicine",

issn = "0033-2917",

publisher = "Cambridge University Press",

number = "6",

}

TY - JOUR

T1 - Interactive impact of childhood maltreatment, depression, and age on cortical brain structure

T2 - Mega-analytic findings from a large multi-site cohort

AU - Tozzi, Leonardo

AU - Garczarek, Lisa

AU - Janowitz, Deborah

AU - Stein, Dan J.

AU - Wittfeld, Katharina

AU - Dobrowolny, Henrik

AU - Lagopoulos, Jim

AU - Hatton, Sean N.

AU - Hickie, Ian B.

AU - Carballedo, Angela

AU - Brooks, Samantha J.

AU - Vuletic, Daniella

AU - Uhlmann, Anne

AU - Veer, Ilya M.

AU - Walter, Henrik

AU - Bülow, Robin

AU - Völzke, Henry

AU - Klinger-König, Johanna

AU - Schnell, Knut

AU - Schoepf, Dieter

AU - Grotegerd, Dominik

AU - Opel, Nils

AU - Dannlowski, Udo

AU - Kugel, Harald

AU - Schramm, Elisabeth

AU - Konrad, Carsten

AU - Kircher, Tilo

AU - Jüksel, Dilara

AU - Nenadić, Igor

AU - Krug, Axel

AU - Hahn, Tim

AU - Steinsträter, Olaf

AU - Redlich, Ronny

AU - Zaremba, Dario

AU - Zurowski, Bartosz

AU - Fu, Cynthia H.Y.

AU - Dima, Danai

AU - Cole, James

AU - Grabe, Hans J.

AU - Connolly, Colm G.

AU - Yang, Tony T.

AU - Ho, Tiffany C.

AU - Lewinn, Kaja Z.

AU - Li, Meng

AU - Groenewold, Nynke A.

AU - Salminen, Lauren E.

AU - Walter, Martin

AU - Simmons, Alan N.

AU - Van Erp, Theo G.M.

AU - Jahanshad, Neda

AU - Baune, Bernhard T.

AU - Van Der Wee, Nic J.A.

AU - Van Tol, Marie Jose

AU - Penninx, Brenda W.J.H.

AU - Hibar, Derrek P.

AU - Thompson, Paul M.

AU - Veltman, Dick J.

AU - Schmaal, Lianne

AU - Frodl, Thomas

N1 - Funding Information: group gratefully acknowledges support from the NIH BD2 K award, U54 EB020403. The infrastructure for the NESDA study (http://www.nesda.nl) is funded through the Geestkracht program of the Netherlands Organisation for Health Research and Development (Zon-Mw, grant number 10-000-1002) and is supported by participating universities (VU University Medical Center, GGZ inGeest, Arkin, Leiden University Medical Center, GGZ Rivierduinen, University Medical Center Groningen) and mental health care organizations, see http://www.nesda.nl. Lianne Schmaal is supported by The Netherlands Brain Foundation Grant number F2014(1)-24 and the Neuroscience Campus Amsterdam Scientific Excellence grant (IPB-SE-15-PSYCH-Schmaal). Funding Information: Financial support. The Münster Neuroimaging Cohort was funded by the German Research Foundation (SFB-TRR58, Projects C09 and Z02 to UD) and the Interdisciplinary Center for Clinical Research (IZKF) of the medical faculty of Münster (grant Dan3/012/17 to UD). FOR2107-Marburg was funded by the German Research Foundation (DFG, grant FOR2107 KI588/ 14-1, KI588/15-1, KI588/14-2, KI588/15-2 to TK, KR3822/5-1 to AK). FOR2107-Münster was funded by the German Research Foundation (DFG, grant FOR2107 HA 7070/2-2 to TH; DA1151/5-1 and DA1151/5-2 to UD). Funding Information: ENIGMA was supported in part by a Consortium grant (U54 EB020403 to PMT, DPH, NJ) from the NIH Institutes contributing to the Big Data to Knowledge (BD2 K) Initiative, and by R01 MH116147 and R56 AG058854. Moreover, an NIH BD2 K award, U54EB020403 to T.G.M. van Erp. London: This paper represents independent research [part] funded by the National Institute for Health Research (NIHR) Biomedical Research Centre at South London and Maudsley NHS Foundation Trust and King’s College London. The views expressed are those of the author(s) and not necessarily those of the NHS, the NIHR or the Department of Health and Social Care. SHIP: The Study of Health in Pomerania (SHIP) is supported by the German Federal Ministry of Education and Research (grants 01ZZ9603, 01ZZ0103, and 01ZZ0403) the Ministry of Cultural Affairs as well as the Social Ministry of the Federal State of Mecklenburg-West Pomerania. MRI scans were supported by Siemens Healthcare, Erlangen, Germany. SHIP-LEGEND was supported by the German Research Foundation (GR1912/5-1). Dublin: The study was supported by a Science Foundation Ireland (SFI) Stokes Professorship Grant to Thomas Frodl. San Francisco: This work was supported by the Brain and Behavior Research Foundation (formerly NARSAD) to T.T.Y.; the National Institute of Mental Health (R01MH085734 to T.T.Y.; K01MH097978 to K.Z.L.; K01MH117442 to T.C.H.) and by the American Foundation for Suicide Prevention (PDF-1-064-13) to T.C.H. Publisher Copyright: Copyright © 2019 Cambridge University Press.

PY - 2020/4/1

Y1 - 2020/4/1

N2 - Background Childhood maltreatment (CM) plays an important role in the development of major depressive disorder (MDD). The aim of this study was to examine whether CM severity and type are associated with MDD-related brain alterations, and how they interact with sex and age.Methods Within the ENIGMA-MDD network, severity and subtypes of CM using the Childhood Trauma Questionnaire were assessed and structural magnetic resonance imaging data from patients with MDD and healthy controls were analyzed in a mega-analysis comprising a total of 3872 participants aged between 13 and 89 years. Cortical thickness and surface area were extracted at each site using FreeSurfer.Results CM severity was associated with reduced cortical thickness in the banks of the superior temporal sulcus and supramarginal gyrus as well as with reduced surface area of the middle temporal lobe. Participants reporting both childhood neglect and abuse had a lower cortical thickness in the inferior parietal lobe, middle temporal lobe, and precuneus compared to participants not exposed to CM. In males only, regardless of diagnosis, CM severity was associated with higher cortical thickness of the rostral anterior cingulate cortex. Finally, a significant interaction between CM and age in predicting thickness was seen across several prefrontal, temporal, and temporo-parietal regions.Conclusions Severity and type of CM may impact cortical thickness and surface area. Importantly, CM may influence age-dependent brain maturation, particularly in regions related to the default mode network, perception, and theory of mind.

AB - Background Childhood maltreatment (CM) plays an important role in the development of major depressive disorder (MDD). The aim of this study was to examine whether CM severity and type are associated with MDD-related brain alterations, and how they interact with sex and age.Methods Within the ENIGMA-MDD network, severity and subtypes of CM using the Childhood Trauma Questionnaire were assessed and structural magnetic resonance imaging data from patients with MDD and healthy controls were analyzed in a mega-analysis comprising a total of 3872 participants aged between 13 and 89 years. Cortical thickness and surface area were extracted at each site using FreeSurfer.Results CM severity was associated with reduced cortical thickness in the banks of the superior temporal sulcus and supramarginal gyrus as well as with reduced surface area of the middle temporal lobe. Participants reporting both childhood neglect and abuse had a lower cortical thickness in the inferior parietal lobe, middle temporal lobe, and precuneus compared to participants not exposed to CM. In males only, regardless of diagnosis, CM severity was associated with higher cortical thickness of the rostral anterior cingulate cortex. Finally, a significant interaction between CM and age in predicting thickness was seen across several prefrontal, temporal, and temporo-parietal regions.Conclusions Severity and type of CM may impact cortical thickness and surface area. Importantly, CM may influence age-dependent brain maturation, particularly in regions related to the default mode network, perception, and theory of mind.

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DO - 10.1017/S003329171900093X

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EP - 1031

JO - Psychological Medicine

JF - Psychological Medicine

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ER -

Interactive impact of childhood maltreatment, depression, and age on cortical brain structure: Mega-analytic findings from a large multi-site cohort

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