The Journal of Clinical Endocrinology & Metabolism, 2021, Vol. 106, No. 3, 750–761
doi:10.1210/clinem/dgaa892
Clinical Research Article
ISSN Print 0021-972X ISSN Online 1945-7197
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Clinical Research Article
Insulin Resistance Is Central to Long-
Term Reversal of Histologic Nonalcoholic
Steatohepatitis After Metabolic Surgery
Maria Francesca Russo,
1,2,
* Erminia Lembo,
1,2,
*
Andrea Mari,
3
Giulia Angelini,
1,2
Ornella Verrastro,
1,2
Giuseppe Nanni,
1,2
Maurizio Pompili,
1,2
Marco Raffaelli,
1,2
Fabio Maria Vecchio,
1,2
Stefan R. Bornstein,
4,5
and
Geltrude Mingrone
1,2,4
1
Fondazione Policlinico Universitario A. Gemelli IRCCS, 00168 Rome, Italy;
2
Università Cattolica del Sacro
Cuore Rome, 00168 Rome, Italy;
3
Institute of Neuroscience, National Research Council, 35127 Padua,
Italy;
4
Division of Diabetes & Nutritional Sciences, Faculty of Life Sciences & Medicine, King’s College
London, SE1 9NH London, UK; and
5
Department of Medicine III, Universitätsklinikum Carl Gustav Carus
an der Technischen Universität Dresden, 01307 Dresden, Germany
ORCiD number: 0000-0003-2021-528X (G. Mingrone).
*M.F.R. and E.L. contributed equally to this work.
Abbreviations: γ-GT, γ-glutamyltransferase; ALT, alanine aminotransferase; APRI, aspartate aminotransferase to
platelets ratio; AST, aspartate aminotransferase; AUC, area under the curve; BPD, biliopancreatic diversion; C-peptide,
connecting peptide; FIB4, Fibrosis-4 score; HDL, high-density lipoprotein; HOMA-IR, Homeostasis Model Assessment of
Insulin Resistance; ISR, insulin secretion rate; LDL, low-density lipoprotein; NAFLD, nonalcoholic fatty liver disease; NAS,
nonalcoholic fatty liver disease activity score; NASH, nonalcoholic steatohepatitis; NFS, nonalcoholic fatty liver disease
fbrosis score; OGTT, oral glucose tolerance test; PLS-DA, partial least squares–discriminant analysis; RCT, randomized
clinical trial; ROC, receiver operating characteristic curve; SAF, steatosis-activity-fbrosis; T2DM, type 2 diabetes mellitus;
VIP, variable importance in the projection.
Received: 1 September 2020; Editorial Decision: 22 November 2020; First Published Online: 28 November 2020; Corrected and
Typeset: 16 January 2021.
Abstract
Context: Nonalcoholic steatohepatitis (NASH) is considered the hepatic counterpart of
metabolic syndrome.
Objective: This work aimed to investigate the determinants of NASH reversal in patients
undergoing biliopancreatic diversion (BPD) in a 5-year follow-up study.
Methods: This prospective study was conducted at Policlinico Universitario Agostino
Gemelli. A total of 37 patients underwent fne-needle liver biopsy during BPD.
Ultrasonography-guided percutaneous liver biopsy was obtained 5 years after the
operation. The primary outcome of our study was histologic NASH reversal at 5-year
follow-up. To better characterize the clinical variables involved in the resolution of NASH,
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