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Contemporary Endocrinology
Series Editor: Leonid Poretsky

Philip S. Zeitler
Kristen J. Nadeau Editors

Insulin
Resistance
Childhood Precursors of Adult Disease
Second Edition
Contemporary Endocrinology
Series Editor
Leonid Poretsky
Division of Endocrinology
Lenox Hill Hospital
New York, NY, USA

More information about this series at http://www.springer.com/series/7680

Philip S. Zeitler • Kristen J. Nadeau
Editors

Insulin Resistance
Childhood Precursors of Adult
Disease

Second Edition
Editors
Philip S. Zeitler Kristen J. Nadeau
Section of Pediatric Endocrinology Department of Pediatrics
Children’s Hospital Colorado Children’s Hospital Colorado
Aurora, CO Aurora, CO
USA USA

ISSN 2523-3785     ISSN 2523-3793 (electronic)

Contemporary Endocrinology
ISBN 978-3-030-25055-3    ISBN 978-3-030-25057-7 (eBook)
https://doi.org/10.1007/978-3-030-25057-7

© Springer Nature Switzerland AG 2020

This work is subject to copyright. All rights are reserved by the Publisher, whether the whole or
part of the material is concerned, specifically the rights of translation, reprinting, reuse of
illustrations, recitation, broadcasting, reproduction on microfilms or in any other physical way,
and transmission or information storage and retrieval, electronic adaptation, computer software,
or by similar or dissimilar methodology now known or hereafter developed.
The use of general descriptive names, registered names, trademarks, service marks, etc. in this
publication does not imply, even in the absence of a specific statement, that such names are
exempt from the relevant protective laws and regulations and therefore free for general use.
The publisher, the authors, and the editors are safe to assume that the advice and information in
this book are believed to be true and accurate at the date of publication. Neither the publisher nor
the authors or the editors give a warranty, expressed or implied, with respect to the material
contained herein or for any errors or omissions that may have been made. The publisher remains
neutral with regard to jurisdictional claims in published maps and institutional affiliations.

This Humana imprint is published by the registered company Springer Nature Switzerland AG
The registered company address is: Gewerbestrasse 11, 6330 Cham, Switzerland
Series Editor Foreword

The concept of insulin resistance was placed on a firm scientific ground by

Rosalyn Yalow and Solomon Berson in their Nobel prize-winning work,
which described the development of radioimmunoassay (the first radioim-
munoassay was for insulin) [1]. The authors demonstrated that circulating
insulin levels in individuals with type 2 diabetes were not low or absent, as
was assumed at the time, but are often increased.
With one-third of the US population developing prediabetes and two-
thirds either overweight or obese, insulin resistance is arguably the most
common disease-related condition in the United States and probably world-
wide. Although pathophysiology of insulin resistance is relatively well under-
stood, its specific causes in individual patients remain unknown (with some
rare exceptions, e.g., in individuals with syndromes of extreme insulin resis-
tance due to the mutations of insulin receptor gene or autoantibodies to the
insulin receptor). This is true even for such common conditions as obesity or
type 2 diabetes mellitus. Further, a diagnosis of insulin resistance is virtually
impossible to make with precision in a clinical setting and is difficult in a
research setting.
When much about insulin resistance remains to be learned, it is useful to
summarize the current state of the art. Because the roots of insulin resistance
are often established in childhood, the current volume, edited by Drs. Philip
S. Zeitler and Kristen J. Nadeau, is an invaluable resource for anyone inter-
ested in pathophysiology, diagnosis, and management of insulin resistance.
The chapters, written by world-class authorities, cover the entire spectrum of
knowledge about insulin resistance including molecular mechanisms of insu-
lin action, genetics, diagnosis, role of environment, puberty, pregnancy, and a
variety of disease states. Exceptionally well written, referenced, and edited,
the book is a welcome addition to the knowledge armamentarium of both
pediatric and adult endocrinologists, as well as clinical investigators and
basic scientists who continue to work tirelessly in order to shed more light on
this common but still mysterious condition.

New York, NY, USA Leonid Poretsky, MD

v
vi Series Editor Foreword

Reference

1. Kahn CR, Roth J. Berson, Yalow, and the JCI: the agony and the ecstasy. J
Clin Invest. 2004;114(8):1051–4.
Preface to the Second Edition

Since the publication of the first edition of this book, there has been substan-
tial progress in the understanding of insulin resistance and β-cell function, as
well as the contribution of these two factors to the pathophysiology of type 2
diabetes and other disorders associated with obesity. In particular, a deeper
understanding of the unique pathophysiology of insulin resistance in child-
hood and the impact of insulin resistance across the lifespan is emerging. This
understanding includes a greater appreciation of the impact of insulin action
on development of body composition in the fetus, child, and adolescent; the
unique impact of puberty and sex steroids; the role of insulin resistance in the
fetus and early life in the programming of glucose metabolism and pancreatic
function; the effect of insulin resistance on development of target organ
abnormalities in the liver, kidney, and heart; and the now-established role of
insulin resistance in the young as a risk for disease in adulthood. In the pro-
cess, there has been increased recognition that, beyond risk for the future,
disorders related to insulin resistance are also having serious metabolic and
cardiorenal impacts resulting in life-altering diseases at a time when indi-
viduals should be reaching their prime years for education, work, and family.
As a reflection that insulin resistance in the young is having both short-term
and long-term effects, we have changed the name of this book to Insulin
Resistance: Childhood Precursors of Adult Disease.
In this second edition, we have again brought together experts in the field
to provide a comprehensive overview and update on a wide variety of topics
related to insulin resistance in youth. In some cases, these contributions are
updated and timely chapters from the first edition. In other cases, we have
added new chapters to address areas not previously covered. The first part of
the edition addresses the clinical presentation and assessment of insulin resis-
tance in youth, as well as a new chapter on insulin resistance in chronic child-
hood disease, an increasing contributor to the clinical picture of insulin
resistance in children. Part II reviews the pathophysiology of insulin resis-
tance in youth, including mechanism of insulin resistance and impact on
metabolism, contributions of the in utero and early childhood environments,
the growing understanding of the relationship between puberty and insulin
resistance, and current perspectives on the role of body composition and ecto-
pic fat. It closes with reviews of the impact of insulin resistance on the heart,
liver, and kidneys. Part III addresses unique clinical settings for insulin resis-
tance in youth, including type 1 diabetes, intrauterine growth retardation, and
adolescent polycystic ovary syndrome. Finally, Part IV focuses on treatment,

vii
viii Preface to the Second Edition

with a discussion of whether insulin resistance itself should be considered a

treatment target, as well as impact of exercise, weight loss medications, and
bariatric surgery.
Insulin resistance continues to grow as a serious public health concern
underlying the leading causes of morbidity and mortality in most of the
world. This problem is increasingly affecting youth and threatens their long-­
term well-being and productivity, as well as boding crippling health-care
costs. While we have made strides in understanding the root causes of insulin
resistance, much remains to be explored in terms of molecular, biochemical,
and physiological aspects of the disorder, as well as the human face reflected
in the epidemiology, and how this understanding can be translated into inter-
vention. This second edition provides perspective on insulin resistance as it
affects individuals across the lifespan. As with the first edition, we hope that
bringing together these updated contributions will continue to spur interest in
the topic on the part of clinicians and researchers, as well as public health
experts and decisionmakers.

Aurora, CO, USA Philip S. Zeitler

 Kristen J. Nadeau
Contents

Part I Definition and Epidemiology

1 Clinical Manifestations of Insulin Resistance in Youth����������������   3

Melinda E. Chen and Tamara S. Hannon
2 Techniques to Assess Insulin Action in Youth�������������������������������� 19
Sara Fleet Michaliszyn and Silva Arslanian
3 Insulin Resistance in Chronic Disease�������������������������������������������� 37
Uri Hamiel and Orit Pinhas-Hamiel

Part II Pathophysiology

4 Molecular Mechanisms of Insulin Resistance ������������������������������ 55

Boris Draznin
5 Insulin Resistance in Pregnancy: Implications for Mother
and Offspring ���������������������������������������������������������������������������������� 67
Teri L. Hernandez, Jacob E. Friedman, and Linda A. Barbour
6 Maternal-Fetal Contributors to Insulin Resistance
Syndrome in Youth�������������������������������������������������������������������������� 95
Jill Landsbaugh Kaar and Dana Dabelea
7 Early Childhood Contributions to Insulin Resistance������������������ 109
David B. Dunger, Burak Salgin, and Ken K. Ong
8 Insulin Resistance in Puberty �������������������������������������������������������� 119
Jennifer E. Sprague, Rachelle Gandica,
and Megan Moriarty Kelsey
9 Adiposity Is the Enemy: Body Composition
and Insulin Sensitivity �������������������������������������������������������������������� 133
Shanlee M. Davis, Vanessa D. Sherk, and Janine Higgins
10 Ectopic Fat and Insulin Resistance in Youth �������������������������������� 155
Giuseppina Rosaria Umano and Sonia Caprio
11 Biomarkers of Insulin Resistance �������������������������������������������������� 169
Kimberly A. Cox-York and Rocio I. Pereira

ix
x Contents

12 Insulin Resistance and Cardiovascular Disease���������������������������� 195

Jessica E. Haley and Elaine M. Urbina
13 The Liver and Insulin Resistance: The Important
Convergence of Endocrinology and Hepatology �������������������������� 207
Charissa Y. Chang, Kerry Whitt, Zhenqi Liu,
and Stephen H. Caldwell
14 Insulin Resistance and the Kidney in Youth���������������������������������� 221
Petter Bjornstad and David Z. Cherney

Part III Unique Models of Insulin Resistance in Youth

15 Intrauterine Growth Restriction and Insulin Resistance������������ 239

Sara E. Pinney and Rebecca A. Simmons
16 Polycystic Ovary Syndrome and Metabolic Syndrome���������������� 255
Anne-Marie Carreau, Marie-Hélène Pesant, and
Jean-Patrice Baillargeon

Part IV Treatment

17 Is Insulin Resistance a Treatment Target?������������������������������������ 277

Thomas Reinehr
18 Exercise in Metabolic Syndrome and Diabetes:
A Central Role for Insulin Sensitivity�������������������������������������������� 293
Irene E. Schauer, Judith G. Regensteiner,
and Jane E. B. Reusch
19 Weight Loss Medications in Adolescents �������������������������������������� 325
Linda L. Buckley, Daniel H. Bessesen, and Philip S. Zeitler
20 Adolescent Metabolic/Bariatric Surgery: Effects on Obesity,
Comorbidities, and Insulin Resistance������������������������������������������ 335
Daniel S. Hsia, Amy Sanghavi Shah, and Thomas Inge

Index �������������������������������������������������������������������������������������������������������� 347

Editors

Philip S. Zeitler, MD, PhD Section of Pediatric Endocrinology, University

of Colorado School of Medicine, Children’s Hospital Colorado, Aurora, CO,
USA
Kristen J. Nadeau, MS, MS Department of Pediatrics, University of
Colorado Anschutz Medical Campus, Children’s Hospital Colorado, Aurora,
CO, USA

xi
Contributors

Silva Arslanian, MD Department of Pediatric Endocrinology, Metabolism

& Diabetes Mellitus, University of Pittsburgh, School of Medicine, Pediatric
Clinical & Translational Research Center, Center for Pediatric Research in
Obesity and Metabolism, Pittsburgh, PA, USA
Jean-Patrice Baillargeon, MD, MSc Department of Medicine, Université
de Sherbrooke, Sherbrooke, QC, Canada
Linda A. Barbour, MD, MSPH Department of Medicine, Division of
Endocrinology, Metabolism, and Diabetes, Department of Obstetrics and
Gynecology, Division of Maternal-Fetal Medicine, University of Colorado,
Aurora, CO, USA
Daniel H. Bessesen, MD Department of Medicine, University of Colorado
Denver School of Medicine, Aurora, CO, USA
Petter Bjornstad, MD Section of Endocrinology, Department of Pediatrics,
Division of Nephrology, Department of Medicine, University of Colorado
School of Medicine, Denver, CO, USA
Linda L. Buckley, MD Swedish Medical Center, Denver Endocrinology/
Diabetes & Thyroid Center PC, Englewood, CO, USA
Stephen H. Caldwell, MD Division of Gastroenterology and Hepatology,
Department of Medicine, University of Virginia Health System, Digestive
Health Center, Charlottesville, VA, USA
Sonia Caprio, MD Department of Pediatrics, Division of Pediatric
Endocrinology, Yale University School of Medicine, New Haven, CT, USA
Anne-Marie Carreau, MD, MSc Department of Medicine, Université de
Sherbrooke, Sherbrooke, QC, Canada
Charissa Y. Chang, MD Liver Disease Practice, Mount Sinai Health
System, New York, NY, USA
Melinda E. Chen, MD, MS Department of Pediatric Endocrinology,
University of Nebraska Medical Center, Children’s Hospital and Medical
Center, Omaha, NE, USA
David Z. Cherney, MD, PhD Department of Medicine, Division of
Nephrology, University Health Network, University of Toronto, Toronto, ON,
Canada
xiii
xiv Contributors

Kimberly A. Cox-York, BS, MS, PhD Department of Food Science and

Human Nutrition, Colorado State University, Fort Collins, CO, USA
Dana Dabelea, MD, PhD Department of Epidemiology and Pediatrics,
Lifecourse Epidemiology of Adiposity and Diabetes (LEAD) Center,
Colorado School of Public Health, University of Colorado Anschutz Medical
Campus, Aurora, CO, USA
Shanlee M. Davis, MD, MS Department of Pediatrics, University of
Colorado Anschutz Medical Campus, Aurora, CO, USA
Boris Draznin, MD, PhD Department of Medicine, Division of
Endocrinology, Metabolism, and Diabetes, University of Colorado, Aurora,
CO, USA
David B. Dunger, MD Department of Paediatrics, University of Cambridge,
Cambridge, UK
Jacob E. Friedman, PhD Department of Pediatrics, Department of
Medicine, Division of Endocrinology, Metabolism, and Diabetes, University
of Colorado, Aurora, CO, USA
Rachelle Gandica, MD Department of Pediatric Endocrinology, Naomi
Berrie Diabetes Center, Columbia University Irving Medical Center, New
York, NY, USA
Jessica E. Haley, MD Department of Pediatrics, Pediatric Cardiology,
University of California San Diego, Rady Children’s Hospital – San Diego,
San Diego, CA, USA
Uri Hamiel, MD Department of Pediatrics, Assaf Harofeh Medical Center,
Zerifin, Israel
Sackler School of Medicine, Tel-Aviv University, Tel Aviv-Yafo, Israel
Tamara S. Hannon, MD, MS Department of Pediatrics, Division of
Pediatric Endocrinology and Diabetology, Indiana University School of
Medicine, Indianapolis, IN, USA
Teri L. Hernandez, PhD, RN Department of Medicine and Nursing,
Division of Endocrinology, Metabolism, and Diabetes, University of
Colorado, Children’s Hospital Colorado, Aurora, CO, USA
Janine Higgins, PhD Department of Pediatrics, University of Colorado
Anschutz Medical Campus, Aurora, CO, USA
Daniel S. Hsia, MD Clinical Trials Unit, Pennington Biomedical Research
Center, Baton Rouge, LA, USA
Thomas Inge, MD, PhD Department of Pediatric Surgery, Children’s
Hospital Colorado, Aurora, CO, USA
Jill Landsbaugh Kaar, PhD Department of Pediatrics, University of
Colorado School of Medicine, Aurora, CO, USA
Megan Moriarty Kelsey, MD, MS Department of Pediatrics, Children’s
Hospital Colorado, University of Colorado School of Medicine, Aurora, CO,
USA
Contributors xv

Zhenqi Liu, MD Division of Endocrinology and Metabolism, Department

of Medicine, University of Virginia School of Medicine, Charlottesville, VA,
USA
Sara Fleet Michaliszyn, PhD Kinesiology and Sport Science, Youngstown
State University, Youngstown, OH, USA
Ken K. Ong, PhD MRC Epidemiology Unit, Department of Paediatrics,
University of Cambridge, Cambridge, UK
Rocio I. Pereira, MD Department of Medicine, Endocrinology, Denver
Health Medical Center, Denver, CO, USA
Marie-Hélène Pesant, MD Department of Medicine, Université de
Sherbrooke, Sherbrooke, QC, Canada
Orit Pinhas-Hamiel, MD Sackler School of Medicine, Tel Aviv University,
Israel, Pediatric Endocrine and Diabetes Unit, Edmond and Lily Safra
Children’s Hospital, Sheba Medical Center, Tel-Hashomer, Israel
Sara E. Pinney, MD, MS Department of Pediatrics, Division of
Endocrinology and Diabetes, Perelman School of Medicine at the University
of Pennsylvania, The Children’s Hospital of Philadelphia, Philadelphia, PA,
USA
Judith G. Regensteiner, PhD Department of Medicine, Division of
Cardiology, Center for Women’s Health Research, and Office of Women in
Medicine and Science, University of Colorado Anschutz Medical Campus,
Aurora, CO, USA
Thomas Reinehr, MD Department of Pediatric Endocrinology, Diabetes
and Nutrition Medicine, Vestische Children’s Hospital, University of Witten/
Herdecke, Datteln, NRW, Germany
Jane E. B. Reusch, MD Department of Medicine, Division of Endocrinology,
Metabolism, and Diabetes, University of Colorado Anschutz Medical Campus
and Rocky Mountain Regional VA Medical Center, Aurora, CO, USA
Burak Salgin, MD Department of Paediatrics, The Rosie Hospital,
Cambridge University Hospitals, Cambridge, UK
Irene E. Schauer, MD, PhD Department of Medicine, Division of
Endocrinology, Metabolism, and Diabetes, University of Colorado Anschutz
Medical Campus and Rocky Mountain Regional VA Medical Center, Aurora,
CO, USA
Amy Sanghavi Shah, MD, MS Department of Pediatrics, University of
Cincinnati, Cincinnati Children’s Hospital Medical Center, Cincinnati, OH,
USA
Vanessa D. Sherk, PhD Department of Medicine, University of Colorado
Anschutz Medical Campus, Aurora, CO, USA
Rebecca A. Simmons, MD Department of Pediatrics, Perelman School of
Medicine at the University of Pennsylvania, The Children’s Hospital of
Philadelphia, Philadelphia, PA, USA
xvi Contributors

Jennifer E. Sprague, MD, PhD Department of Pediatrics, Washington

University, St. Louis, MO, USA
Giuseppina Rosaria Umano, MD Department of Pediatrics, Division of
Pediatric Endocrinology, Yale University School of Medicine, New Haven,
CT, USA
Department of the Woman, the Child, of General and Specialized Surgery,
University of Campania “Luigi Vanvitelli”, Naples, Italy
Elaine M. Urbina, MD, MS Department of Pediatric Preventive Cardiology,
Cincinnati Children’s Hospital Medical Center, Cincinnati, OH, USA
Kerry Whitt, MD RMG Gastroenterology, Raleigh, NC, USA
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