A methodological checklist for fMRI drug cue reactivity studies: development and expert consensus

Hamed Ekhtiari, Mehran Zare-Bidoky, Arshiya Sangchooli, Amy C. Janes, Marc J. Kaufman, Jason A. Oliver, James J. Prisciandaro, Torsten Wüstenberg, Raymond F. Anton, Patrick Bach, Alex Baldacchino, Anne Beck, James M. Bjork, Judson Brewer, Anna Rose Childress, Eric D. Claus, Kelly E. Courtney, Mohsen Ebrahimi, Francesca M. Filbey, Dara G. GhahremaniPeyman Ghobadi Azbari, Rita Z. Goldstein, Anna E. Goudriaan, Erica N. Grodin, J. Paul Hamilton, Colleen A. Hanlon, Peyman Hassani-Abharian, Andreas Heinz, Jane E. Joseph, Falk Kiefer, Arash Khojasteh Zonoozi, Hedy Kober, Rayus Kuplicki, Qiang Li, Edythe D. London, Joseph McClernon, Hamid R. Noori, Max M. Owens, Martin P. Paulus, Irene Perini, Marc Potenza, Stéphane Potvin, Lara Ray, Joseph P. Schacht, Dongju Seo, Rajita Sinha, Michael N. Smolka, Rainer Spanagel, Vaughn R. Steele, Elliot A. Stein, Sabine Steins-Loeber, Susan F. Tapert, Antonio Verdejo-Garcia, Sabine Vollstädt-Klein, Reagan R. Wetherill, Stephen J. Wilson, Katie Witkiewitz, Kai Yuan, Xiaochu Zhang, Anna Zilverstand

Research output: Contribution to journalReview articlepeer-review

3 Scopus citations

Abstract

Cue reactivity is one of the most frequently used paradigms in functional magnetic resonance imaging (fMRI) studies of substance use disorders (SUDs). Although there have been promising results elucidating the neurocognitive mechanisms of SUDs and SUD treatments, the interpretability and reproducibility of these studies is limited by incomplete reporting of participants’ characteristics, task design, craving assessment, scanning preparation and analysis decisions in fMRI drug cue reactivity (FDCR) experiments. This hampers clinical translation, not least because systematic review and meta-analysis of published work are difficult. This consensus paper and Delphi study aims to outline the important methodological aspects of FDCR research, present structured recommendations for more comprehensive methods reporting and review the FDCR literature to assess the reporting of items that are deemed important. Forty-five FDCR scientists from around the world participated in this study. First, an initial checklist of items deemed important in FDCR studies was developed by several members of the Enhanced NeuroImaging Genetics through Meta-Analyses (ENIGMA) Addiction working group on the basis of a systematic review. Using a modified Delphi consensus method, all experts were asked to comment on, revise or add items to the initial checklist, and then to rate the importance of each item in subsequent rounds. The reporting status of the items in the final checklist was investigated in 108 recently published FDCR studies identified through a systematic review. By the final round, 38 items reached the consensus threshold and were classified under seven major categories: ‘Participants’ Characteristics’, ‘General fMRI Information’, ‘General Task Information’, ‘Cue Information’, ‘Craving Assessment Inside Scanner’, ‘Craving Assessment Outside Scanner’ and ‘Pre- and Post-Scanning Considerations’. The review of the 108 FDCR papers revealed significant gaps in the reporting of the items considered important by the experts. For instance, whereas items in the ‘General fMRI Information’ category were reported in 90.5% of the reviewed papers, items in the ‘Pre- and Post-Scanning Considerations’ category were reported by only 44.7% of reviewed FDCR studies. Considering the notable and sometimes unexpected gaps in the reporting of items deemed to be important by experts in any FDCR study, the protocols could benefit from the adoption of reporting standards. This checklist, a living document to be updated as the field and its methods advance, can help improve experimental design, reporting and the widespread understanding of the FDCR protocols. This checklist can also provide a sample for developing consensus statements for protocols in other areas of task-based fMRI.

Original languageEnglish (US)
Pages (from-to)567-595
Number of pages29
JournalNature Protocols
Volume17
Issue number3
DOIs
StatePublished - Mar 2022

Bibliographical note

Funding Information:
R.F.A. is supported by the National Institute on Alcohol Abuse and Alcoholism (NIAAA) P50 AA010761. P.B. is supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)—Project-ID 402170461—TRR 265. A.B. is supported by the DFG – Project-ID 402170461 – TRR 265. K.E.C. is supported by the California Tobacco-Related Disease Research Grant Program of the University of California grant number T30IP0962. H.E. is supported by the Laureate Institute for Brain Research (LIBR), Warren K. Family Foundation, Oklahoma Center for Advancement of Science and Technologies (OCAST, #HR18-139) and Brain and Behavior Foundation (NARSAD Young Investigator Award #27305). F.M.F. is supported by the National Institute on Drug Abuse (NIDA) grants R01 DA030344 and R21DA044465. R.Z.G. is supported by NIDA grants R01DA041528, R01DA048301 and R01DA047851 and NCCIH grant R01AT010627. E.N.G. is supported by NIAAA grant F32AA027699. A.H. is supported by the DFG – Project-ID 402170461 – TRR 265. A.C.J. is supported by NIH grants R01DA039135 and K02DA042987. F.K. is supported by the DFG—Project-ID 402170461—TRR 265. M.J.K. is supported by NIH grant R01 DA041866. H.R.N. is supported by the Bundesministerium für Bildung und Forschung (e:Med program: FKZ: 01ZX1503 and 01ZX1909B), the DFG—Project-ID 402170461—TRR 265, and Shanghai Municipal Science and Technology Major project (grant 2019SHZDZX02). J.A.O. is supported by NIDA grant K23DA042898. S.P. is holder of the Eli Lilly Canada Chair on schizophrenia research. J.P.S. is supported by NIAAA grants R01 AA027765 and R01 AA026859. D.S. is supported by NIH grants R01AA026844 and K08AA023545. M.N.S is supported by the DFG—Project-ID 402170461—TRR 265. R.S is supported by the DFG—Project-ID 402170461—TRR 265. V.R.S. is partially funded by NIDA grant K12 DA000167. S.F.T. is supported by NIAAA grants U01 AA021692 and U24 AA021695 and NIDA grants U01 DA041089 and U24 DA041147. A.V.-G. is supported by the Australian Medical Research Future Fund (MRF1141214). S.V.-K. is supported by the DFG—Project-ID 40217046—TRR 265, Project ID-421888313, Project-ID 437718741 and Project-ID 324164820. R.R.W. is supported by NIH grants K23AA023894, R01DA040670, and R21HL144673. S.J.W. is supported by NIH grants R01DA041438 and R21DA045853. K.W. is supported by NIAAA grants R01AA023665 and R01AA022328. K.Y. is supported by the National Natural Science Foundation of China (Grant No. 81871426). A.Z. is supported by NIDA grants P30 DA048742 and R01DA047851. The views presented in this paper represent those of the authors and not necessarily those of the funding agencies.

Funding Information:
R.F.A. is supported by the National Institute on Alcohol Abuse and Alcoholism (NIAAA) P50 AA010761. P.B. is supported by the Deutsche Forschungsgemeinschaft (DFG, German Research Foundation)—Project-ID 402170461—TRR 265. A.B. is supported by the DFG – Project-ID 402170461 – TRR 265. K.E.C. is supported by the California Tobacco-Related Disease Research Grant Program of the University of California grant number T30IP0962. H.E. is supported by the Laureate Institute for Brain Research (LIBR), Warren K. Family Foundation, Oklahoma Center for Advancement of Science and Technologies (OCAST, #HR18-139) and Brain and Behavior Foundation (NARSAD Young Investigator Award #27305). F.M.F. is supported by the National Institute on Drug Abuse (NIDA) grants R01 DA030344 and R21DA044465. R.Z.G. is supported by NIDA grants R01DA041528, R01DA048301 and R01DA047851 and NCCIH grant R01AT010627. E.N.G. is supported by NIAAA grant F32AA027699. A.H. is supported by the DFG – Project-ID 402170461 – TRR 265. A.C.J. is supported by NIH grants R01DA039135 and K02DA042987. F.K. is supported by the DFG—Project-ID 402170461—TRR 265. M.J.K. is supported by NIH grant R01 DA041866. H.R.N. is supported by the Bundesministerium für Bildung und Forschung (e:Med program: FKZ: 01ZX1503 and 01ZX1909B), the DFG—Project-ID 402170461—TRR 265, and Shanghai Municipal Science and Technology Major project (grant 2019SHZDZX02). J.A.O. is supported by NIDA grant K23DA042898. S.P. is holder of the Eli Lilly Canada Chair on schizophrenia research. J.P.S. is supported by NIAAA grants R01 AA027765 and R01 AA026859. D.S. is supported by NIH grants R01AA026844 and K08AA023545. M.N.S is supported by the DFG—Project-ID 402170461—TRR 265. R.S is supported by the DFG—Project-ID 402170461—TRR 265. V.R.S. is partially funded by NIDA grant K12 DA000167. S.F.T. is supported by NIAAA grants U01 AA021692 and U24 AA021695 and NIDA grants U01 DA041089 and U24 DA041147. A.V.-G. is supported by the Australian Medical Research Future Fund (MRF1141214). S.V.-K. is supported by the DFG—Project-ID 40217046—TRR 265, Project ID-421888313, Project-ID 437718741 and Project-ID 324164820. R.R.W. is supported by NIH grants K23AA023894, R01DA040670, and R21HL144673. S.J.W. is supported by NIH grants R01DA041438 and R21DA045853. K.W. is supported by NIAAA grants R01AA023665 and R01AA022328. K.Y. is supported by the National Natural Science Foundation of China (Grant No. 81871426). A.Z. is supported by NIDA grants P30 DA048742 and R01DA047851. The views presented in this paper represent those of the authors and not necessarily those of the funding agencies.

Funding Information:
R.F.A. is chair of the American Society of Clinical Psychopharmacology’s Alcohol Clinical Trials Initiative (ACTIVE Group), which has received support in the past 36 months from the following: Alkermes, Amygdala Neurosciences, Arbor Pharmaceuticals, Dicerna, Ethypharm, Indivior, Lundbeck, Mitsubishi and Otsuka. He has been a recent consultant for Allergan, Alkermes, Dicerna, Insys, Laboratorio Pharmaceutico and Life Technologies and has received grant funding from Laboratorio Pharmaceutico. A.C.J. consults for Axial Biotherapeutics. M.P.P. consulted for and advised the Addiction Policy Forum, Game Day Data, AXA, Idorsia and Opiant/Lakelight Therapeutics; received research support from the Mohegan Sun Casino and the National Center for Responsible Gaming (now the International Center for Responsible Gaming); consulted for legal and gambling entities on issues related to impulse-control and addictive disorders; has given academic lectures in grand rounds, Continuing Medical Education events and other clinical/scientific venues; and has generated books or chapters for publishers of mental health texts. J.P.S. has consulted for and received grant funding from Laboratorio Farmaceutico CT. The other authors declare no competing interests.

Publisher Copyright:
© 2021, The Author(s), under exclusive licence to Springer Nature Limited.

PubMed: MeSH publication types

  • Journal Article
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

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