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Published in: Digestive Diseases and Sciences 2/2020

01-02-2020 | Nausea | Original Article

Central Nervous System Mechanisms of Nausea in Gastroparesis: An fMRI-Based Case–Control Study

Authors: Phillip Snodgrass, Hugo Sandoval, Vince D. Calhoun, Luis Ramos-Duran, Gengqing Song, Yan Sun, Ben Alvarado, Mohammad Bashashati, Irene Sarosiek, Richard W. McCallum

Published in: Digestive Diseases and Sciences | Issue 2/2020

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Abstract

Background/Aims

Nausea is a major complaint of gastroparesis (GP), and the pathophysiology of this condition is poorly understood. Therefore, this study utilized fMRI to investigate the possible central nervous system (CNS) mechanisms of nausea in 10 GP patients versus 8 healthy controls (HCs).

Methods

Nausea severity was assessed on a 0–10 scale and presented as mean ± SD. Nausea was increased from baseline utilizing up to 30 min of visual stimulation (VS). Functional network connectivity was measured with fMRI at baseline and after 30 min of VS. fMRI data were preprocessed using statistical parametric mapping software. Thirty-four independent components were identified as meaningful resting-state networks (RSNs) by group independent component analysis. The Functional Network Connectivity (FNC) among 5 RSNs considered important in CNS nausea mechanisms was calculated as the Pearson’s pairwise correlation.

Results

Baseline nausea score in GP patients was 2.7 ± 2.0 and increased to 7.0 ± 1.5 after stimulation (P < 0.01). In HCs nausea scores did not increase from baseline after stimulus (0.3 ± 0.5). When comparing GP patients to HCs after VS, a significant reduction (P < 0.001) in bilateral insula network connectivity compared to the right insula network was detected. No significant differences in connectivity were noted among the other RSNs. Additionally, the average gray matter volume was non-significantly reduced in the insula in GP patients compared to HC.

Conclusions

The insula connectivity network is impaired in nauseated GP patients. This phenomenon could explain the susceptibility of GP patients to nausea or may have resulted from a state of chronic nausea.
Literature
1.
go back to reference Sarosiek I, Song G, Sun Y, et al. Central and peripheral effects of transcutaneous acupuncture treatment for nausea in patients with diabetic gastroparesis. J Neurogastroenterol Motil. 2017;23:245–253.CrossRef Sarosiek I, Song G, Sun Y, et al. Central and peripheral effects of transcutaneous acupuncture treatment for nausea in patients with diabetic gastroparesis. J Neurogastroenterol Motil. 2017;23:245–253.CrossRef
2.
go back to reference Camilleri M, Parkman HP, Shafi MA, Abell TL, Gerson L. Clinical guideline: management of gastroparesis. Am J Gastroenterol. 2013;108:18–38.CrossRef Camilleri M, Parkman HP, Shafi MA, Abell TL, Gerson L. Clinical guideline: management of gastroparesis. Am J Gastroenterol. 2013;108:18–38.CrossRef
3.
go back to reference Parkman H, McCallum R. Gastroparesis: Pathophysiology, Presentation, and Treatment. New York: Humana Press; 2012.CrossRef Parkman H, McCallum R. Gastroparesis: Pathophysiology, Presentation, and Treatment. New York: Humana Press; 2012.CrossRef
4.
go back to reference Bashashati M, McCallum RW. Is interstitial cells of cajal-opathy present in gastroparesis? J Neurogastroenterol Motil. 2015;21:486–493.CrossRef Bashashati M, McCallum RW. Is interstitial cells of cajal-opathy present in gastroparesis? J Neurogastroenterol Motil. 2015;21:486–493.CrossRef
5.
go back to reference Napadow V, Sheehan JD, Kim J, et al. The brain circuitry underlying the temporal evolution of nausea in humans. Cereb Cortex. 2013;23:806–813.CrossRef Napadow V, Sheehan JD, Kim J, et al. The brain circuitry underlying the temporal evolution of nausea in humans. Cereb Cortex. 2013;23:806–813.CrossRef
6.
go back to reference Toschi N, Kim J, Sclocco R, et al. Motion sickness increases functional connectivity between visual motion and nausea-associated brain regions. Auton Neurosci. 2017;202:108–113.CrossRef Toschi N, Kim J, Sclocco R, et al. Motion sickness increases functional connectivity between visual motion and nausea-associated brain regions. Auton Neurosci. 2017;202:108–113.CrossRef
7.
go back to reference Abell TL, Camilleri M, Donohoe K, et al. Consensus recommendations for gastric emptying scintigraphy: a joint report of the American Neurogastroenterology and Motility Society and the Society of Nuclear Medicine. J Nucl Med Technol. 2008;36:44–54.CrossRef Abell TL, Camilleri M, Donohoe K, et al. Consensus recommendations for gastric emptying scintigraphy: a joint report of the American Neurogastroenterology and Motility Society and the Society of Nuclear Medicine. J Nucl Med Technol. 2008;36:44–54.CrossRef
8.
go back to reference Kiernan BD, Soykan I, Lin Z, Dale A, McCallum RW. A new nausea model in humans produces mild nausea without electrogastrogram and vasopressin changes. Neurogastroenterol Motil. 1997;9:257–263.CrossRef Kiernan BD, Soykan I, Lin Z, Dale A, McCallum RW. A new nausea model in humans produces mild nausea without electrogastrogram and vasopressin changes. Neurogastroenterol Motil. 1997;9:257–263.CrossRef
9.
go back to reference Freire L, Roche A, Mangin JF. What is the best similarity measure for motion correction in fMRI time series? IEEE Trans Med Imaging. 2002;21:470–484.CrossRef Freire L, Roche A, Mangin JF. What is the best similarity measure for motion correction in fMRI time series? IEEE Trans Med Imaging. 2002;21:470–484.CrossRef
10.
go back to reference Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1994;2:189–210.CrossRef Friston KJ, Holmes AP, Worsley KJ, Poline JP, Frith CD, Frackowiak RSJ. Statistical parametric maps in functional imaging: a general linear approach. Hum Brain Mapp. 1994;2:189–210.CrossRef
11.
go back to reference Calhoun VD, Adali T, Pearlson GD, Pekar JJ. A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp. 2001;14:140–151.CrossRef Calhoun VD, Adali T, Pearlson GD, Pekar JJ. A method for making group inferences from functional MRI data using independent component analysis. Hum Brain Mapp. 2001;14:140–151.CrossRef
12.
go back to reference Allen EA, Erhardt EB, Damaraju E, et al. A baseline for the multivariate comparison of resting-state networks. Frontiers Syst Neurosci. 2011;5:2. Allen EA, Erhardt EB, Damaraju E, et al. A baseline for the multivariate comparison of resting-state networks. Frontiers Syst Neurosci. 2011;5:2.
13.
go back to reference Erhardt EB, Rachakonda S, Bedrick EJ, Allen EA, Adali T, Calhoun VD. Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp. 2011;32:2075–2095.CrossRef Erhardt EB, Rachakonda S, Bedrick EJ, Allen EA, Adali T, Calhoun VD. Comparison of multi-subject ICA methods for analysis of fMRI data. Hum Brain Mapp. 2011;32:2075–2095.CrossRef
14.
go back to reference Meda SA, Giuliani NR, Calhoun VD, et al. A large scale (N = 400) investigation of gray matter differences in schizophrenia using optimized voxel-based morphometry. Schizophr Res. 2008;101:95–105.CrossRef Meda SA, Giuliani NR, Calhoun VD, et al. A large scale (N = 400) investigation of gray matter differences in schizophrenia using optimized voxel-based morphometry. Schizophr Res. 2008;101:95–105.CrossRef
15.
go back to reference Robinson S, Basso G, Soldati N, et al. A resting state network in the motor control circuit of the basal ganglia. BMC Neurosci. 2009;10:137.CrossRef Robinson S, Basso G, Soldati N, et al. A resting state network in the motor control circuit of the basal ganglia. BMC Neurosci. 2009;10:137.CrossRef
16.
go back to reference Cordes D, Haughton VM, Arfanakis K, et al. Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. AJNR Am J Neuroradiol. 2001;22:1326–1333.PubMed Cordes D, Haughton VM, Arfanakis K, et al. Frequencies contributing to functional connectivity in the cerebral cortex in “resting-state” data. AJNR Am J Neuroradiol. 2001;22:1326–1333.PubMed
17.
go back to reference Ashburner J, Friston KJ. Unified segmentation. NeuroImage. 2005;26:839–851.CrossRef Ashburner J, Friston KJ. Unified segmentation. NeuroImage. 2005;26:839–851.CrossRef
Metadata
Title
Central Nervous System Mechanisms of Nausea in Gastroparesis: An fMRI-Based Case–Control Study
Authors
Phillip Snodgrass
Hugo Sandoval
Vince D. Calhoun
Luis Ramos-Duran
Gengqing Song
Yan Sun
Ben Alvarado
Mohammad Bashashati
Irene Sarosiek
Richard W. McCallum
Publication date
01-02-2020
Publisher
Springer US
Keyword
Nausea
Published in
Digestive Diseases and Sciences / Issue 2/2020
Print ISSN: 0163-2116
Electronic ISSN: 1573-2568
DOI
https://doi.org/10.1007/s10620-019-05766-5

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