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HYPOXIC RESPIRATORY
FAILURE IN THE
NEWBORN
HYPOXIC RESPIRATORY
FAILURE IN THE
NEWBORN

From Origins to Clinical Management

Edited by
Shyamala Dakshinamurti

Section Editors
Steven H. Abman
Po-Yin Cheung
Satyan Lakshminrusimha
Patrick J. McNamara
William K. Milsom
CRC Press
Boca Raton and London
First edition published 2022

by CRC Press
6000 Broken Sound Parkway NW, Suite 300, Boca Raton, FL 33487-2742
and by CRC Press

2 Park Square, Milton Park, Abingdon, Oxon, OX14 4RN

© 2022 Taylor & Francis Group, LLC

CRC Press is an imprint of Taylor & Francis Group, LLC

This book contains information obtained from authentic and highly regarded sources. While all reasonable efforts
have been made to publish reliable data and information, neither the author[s] nor the publisher can accept any legal
responsibility or liability for any errors or omissions that may be made. The publishers wish to make clear that any
views or opinions expressed in this book by individual editors, authors or contributors are personal to them and do
not necessarily reflect the views/opinions of the publishers. The information or guidance contained in this book is
intended for use by medical, scientific or health-care professionals and is provided strictly as a supplement to the
medical or other professional’s own judgement, their knowledge of the patient’s medical history, relevant manufac-
turer’s instructions and the appropriate best practice guidelines. Because of the rapid advances in medical science, any
information or advice on dosages, procedures or diagnoses should be independently verified. The reader is strongly
urged to consult the relevant national drug formulary and the drug companies’ and device or material manufactur-
ers’ printed instructions, and their websites, before administering or utilizing any of the drugs, devices or materials
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particular individual. Ultimately it is the sole responsibility of the medical professional to make his or her own profes-
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Trademark Notice: Product or corporate names may be trademarks or registered trademarks and are used only for
identification and explanation without intent to infringe.

“Copyright Satyan Lakshminrusimha, used with permission”, for figures provided by Dr. Satyan Lakshminrusimha.

ISBN: 9780367493998 (hbk)

ISBN: 9781032078182 (pbk)
ISBN: 9780367494018 (ebk)

DOI: 10.1201/9780367494018

Typeset in Warnock Pro

by KnowledgeWorks Global Ltd.
 CONTENTS

Preface..................................................................................................................................................................................................................................vii
Editor.................................................................................................................................................................................................................................. viii
Section Editors....................................................................................................................................................................................................................ix
Contributors......................................................................................................................................................................................................................... x

Introduction.............................................................................................................................................................................................................. 1
Shyamala Dakshinamurti, William K. Milsom, Satyan Lakshminrusimha, Steven H. Abman, Po-Yin Cheung and
Patrick J. McNamara

Part 1: THE ORIGINS OF HYPOXIA TOLERANCE

Edited by William K. Milsom
The Human Fetus and Metabolic Adaptations to Hypoxia............................................................................................................................ 6
Dominique Singer
Hypoxia as a Neuroinflammatory Stimulus during Development.............................................................................................................13
Peter M. MacFarlane and Allison S. Osborne
Human Adaptations to High Altitude..............................................................................................................................................................19
Tatum Simonson
Fetal Llama Adaptation to Altitude in the Andean Altiplano.....................................................................................................................24
Aníbal J. Llanos, Germán Ebensperger, Emilio A. Herrera, Roberto V. Reyes and María Serón-Ferré
Neonates of Burrowing and Hibernating Mammals: Metabolic and Respiratory Adaptations to Hypoxia.....................................28
Yvonne A. Dzal and William K. Milsom
Diving Response and Hypoxia in Deep Sea Mammals.................................................................................................................................34
Allyson Hindle
The Phylogeny and Ontogeny of Cardiorespiratory Coupling in Vertebrates and Its
Relevance to Noninvasive Monitoring of the Human Fetus........................................................................................................................39
Edwin W. Taylor and Harry Gee

Part 2: FETAL HYPOXIA AND NEONATAL TRANSITION

Edited by Satyan Lakshminrusimha
Fetal and Neonatal Oxygen Environment........................................................................................................................................................46
Payam Vali, Robin H. Steinhorn and Satyan Lakshminrusimha
Fetal Oxygenation during Maternal Hypoxic Illness....................................................................................................................................51
Fabiana Postolow and Shyamala Dakshinamurti
Hemodynamics of the Circulatory Transition................................................................................................................................................57
Graeme R. Polglase, Martin Kluckow, Andrew W. Gill and Stuart B. Hooper
Oxygen during Postnatal Stabilization.............................................................................................................................................................62
Maximo Vento and Ola D. Saugstad

Part 3: BIOLOGY OF HYPOXIC RESPIRATORY FAILURE IN THE NEONATE

Edited by Steven H. Abman
Hypoxia and Pulmonary Artery Structure......................................................................................................................................................68
Csaba Galambos and Steven H. Abman
Animal Models of PPHN and Vasoconstrictor Signaling in Hypoxia....................................................................................................... 74
Candice D. Fike and Judy L. Aschner
Hypoxia and Endothelial Dysfunction in the Lung.......................................................................................................................................80
Emily Callan and Girija Ganesh Konduri
Effects of Hypoxia on Pulmonary Vascular Smooth Muscle Contraction and Relaxation...................................................................87
Shyamala Dakshinamurti, Anjali Y. Bhagirath and Robert P. Jankov
Cellular Oxygen Sensing, Mitochondrial Oxygen Sensing and Reactive Oxygen Species...................................................................96
Jason Boehme and Emin Maltepe

v
vi Contents

Reactive Oxygen Species Signaling in Animal Models of Pulmonary Hypertension..........................................................................101

Stephen Wedgwood, Satyan Lakshminrusimha and Robin H. Steinhorn
Hypoxia, Myocardial Metabolic Adaptation, and Right Ventricular Performance..............................................................................106
Mark K. Friedberg
Hypoxic Remodeling of Neonatal Pulmonary Artery and Myocardium................................................................................................111
Hui Zhang, R. Dale Brown, Jason Williams, Cassidy Delaney and Kurt R. Stenmark
Hypoxia-Induced Epigenetic Mechanisms of Pulmonary Hypertension...............................................................................................119
Kurt H. Albertine

Part 4: HYPOXIA AND COLLATERAL DAMAGE

Edited by Po-Yin Cheung
The Effects of Hypoxia Ischemia on the Term Brain, and a Strategic Approach..................................................................................126
Aravanan Anbu Chakkarapani and Nicola J. Robertson
Effects of Hypoxia on Cerebral Perfusion and the Blood-Brain Barrier.................................................................................................135
Divyen K. Shah, W. L. Amelia Lee, David F. Wertheim and Stephen T. Kempley
Effects of Hypoxia on Airway, Alveolar Function, and Respiration.........................................................................................................142
Y.S. Prakash, Christina M. Pabelick and Peter M. MacFarlane
Hypoxic Respiratory Failure and the Neonatal Kidney..............................................................................................................................148
Catherine Morgan and Po-Yin Cheung
The Effect of Hypoxia on Intestinal Function...............................................................................................................................................152
Eric B. Ortigoza and Josef Neu
Effects of Hypoxia on Perinatal Drug Disposition.......................................................................................................................................155
Karel Allegaert, Anne Smits and Pieter Annaert
Anesthetic Considerations for the Neonate with Hypoxic Respiratory Failure....................................................................................160
M. Ruth Graham

Part 5: DIAGNOSIS AND MANAGEMENT OF NEONATAL HYPOXIC RESPIRATORY FAILURE

Edited by Patrick J. McNamara
Epidemiology and Outcomes of Infants with Hypoxemic Respiratory Failure.....................................................................................168
Souvik Mitra, Roberta L. Keller and Prakesh S. Shah
Clinical Evaluation of Hypoxic Respiratory Failure....................................................................................................................................177
Yasser Elsayed and Shyamala Dakshinamurti
Diagnosis of Pulmonary Hypertension by Echocardiography..................................................................................................................184
Danielle R. Rios, Patrick J. McNamara and Regan E. Giesinger
Right Ventricular Performance and Ventricular Interdependence in Hypoxia.....................................................................................193
Afif El Khuffash and Philip T. Levy
Ventilation Strategies in Neonatal Hypoxemic Respiratory Failure........................................................................................................199
Bradley A. Yoder, Michelle J. Yang, Nicholas R. Carr and Martin Keszler
Pulmonary Hypertension Phenotypes in the Newborn............................................................................................................................. 208
Regan E. Giesinger, John P. Kinsella, Steven H. Abman and Patrick J. McNamara
Special Consideration: HRF in Congenital Diaphragmatic Hernia.........................................................................................................216
Gabriel Altit, Jason Gien, Nolan DeLeon and Richard Keijzer
Special Consideration: Hypoxemic Respiratory Failure among Patients with Hypoxic Ischemic Encephalopathy.....................224
Arvind Sehgal, Satyan Lakshminrusimha and Regan E. Giesinger
Special Consideration: HRF in the Preterm..................................................................................................................................................233
Michelle Baczynski, Amish Jain and Dany E. Weisz
Hypoxemic Respiratory Failure: Neonatal Cases.........................................................................................................................................238
Adrianne Rahde Bischoff, Faith Zhu, Amish Jain and Patrick J. McNamara

Index.................................................................................................................................................................................................................................. 246
 PREFACE

Babies with hypoxic respiratory failure were always the sickest in and drawing together international expertise in diagnosis and
the newborn ICU. As a neonatology trainee, I would sit at their treatment. I am grateful to my august co-editors for their tre-
bedsides on call nights, watching their seesawing oxygen satura- mendous insights and enthusiasm in bringing this collection of
tions, all our whirring, thumping machines a poor substitute for knowledge together. And as always, delighted and illuminated by
the safety and sanity of the uterus; willing their fist-sized hearts Satyan Lakshminrusimha’s illustrations.
to pump a little longer, while we figured out a better way to push It must be acknowledged that this book was conceived before,
oxygen into them. but written during the COVID-19 pandemic. There has been no
Yet, at these same oxygen levels, a fetus would have thrived. scientific connection established between COVID and neonatal
What failed these infants was the elemental transition process pulmonary hypertension. But there is an affective connection, in
from fetus to newborn; the key to be born and to live in this world. writing about hypoxic respiratory failure at a crystalline moment
The genesis of this book can be traced back to those roller- when the world is struggling with the toll of hypoxic respiratory
coaster call nights. Also to the writings of evo-devo stalwarts failure. I thank all the contributing authors for their commitment
Stephen Jay Gould and Sean Carroll; to serendipitous lectures to this project despite this pressure.
by the inimitable John West on how the elephant lost its pleu- Every book requires a village; in particular, the organizational
ral space, and Paul Ponganis on the origins of the diving reflex, skills of project managers Nathalie Buissé and Sophia Mbabaali
which felt like bathing one’s brain in pure logic; and a chance from the George & Fay Yee Centre for Healthcare Innovation, and
meeting with Bill Milsom on a mountain in Mongolia. Clear con- the Medical Sciences editorial desk at Taylor & Francis/CRC Press.
nections can be made from human evolution to the process of I thank my family for their support during the compilation
our emergence as creatures capable of independent life. The poet of this volume, including eagle-eyed proofreading, and for their
Mary Oliver urged, Pay attention / Be astonished / Tell about it. gifts of science, mountains and words.
This applies to scientists and clinicians too. There is a compelling Half a century ago, my cousin Sanjay died of hypoxic respira-
poetry to physiology that lurks beneath the myriad details. tory failure soon after birth. How much we have learned since
Gathered here is a collection of reviews by masters in their then. To him and every blue baby since, this effort is in memory.
fields, highlighting the pathways of hypoxia and pulmonary
hypertension from the population to the organism and the cell Shyamala Dakshinamurti

vii
 EDITOR

Dr Shyamala Dakshinamurti is a neonatologist and biomedi- organizer of the annual Canadian National Perinatal Research
cal researcher, Professor of Pediatrics and Physiology at the Meeting. Dr Dakshinamurti’s research is on the hemodynamics
University of Manitoba, Canada, and member of the Biology of the neonatal pulmonary circuit and the physiology of hypoxia
of Breathing theme, Children’s Hospital Research Institute during circulatory transition. She is also a writer interested in sci-
of Manitoba. She is research director for the University of ence communication.
Manitoba’s Neonatology fellowship program, and a scientific

viii
 SECTION EDITORS

Dr Steven H. Abman is Professor of Pediatrics and Director of and has developed mobile apps of neonatal illustrations and
the Pediatric Heart Lung Center at the University of Colorado infographics.
Anschutz School of Medicine and the Children’s Hospital
Colorado, USA. Having trained in Pediatric Pulmonary and Dr Patrick J. McNamara is a staff neonatologist and Director
Critical Care Medicine, Dr. Abman has had a long-standing of the Division of Neonatology at the University of Iowa Stead
interest in the developing lung circulation and pulmonary Family Children’s Hospital and Professor of Pediatrics and
hypertension in diverse settings, as reflected by his clinical and Internal Medicine, University of Iowa, USA. He is the cur-
laboratory-oriented research. He is currently Director of the rent chair of the PanAmerican Hemodynamic Collaborative,
Pediatric Pulmonary Hypertension Network (PPHNet), Executive Pediatric Academic Society Neonatal Hemodynamics Advisory
Vice-Chairman for the BPD Collaborative and President of the and Neonatal Hemodynamics (TnECHO) Special Interest Group
American Pediatric Society. at the American Society of Echocardiography. His clinical and
research interests include myocardial performance in the set-
Dr Po-Yin Cheung is a neonatologist of the Northern Alberta tings of a hemodynamically significant ductus arteriosus, pulmo-
Neonatal Program of Alberta Health Services and a full Professor nary hypertension, and targeted neonatal echocardiography.
in the Departments of Pediatrics, Pharmacology and Surgery at
the University of Alberta, Canada. He is also an Honorary Clinical Dr William K. Milsom is a comparative physiologist and
Professor of the Department of Paediatrics and Adolescent Emeritus Professor of Zoology at the University of British
Medicine at the University of Hong Kong and Honorary Consultant Columbia, Canada, best known as an authority on the evolu-
at the NICU of the HKU-Shenzhen Hospital. Dr. Cheung is a tion of respiratory processes in vertebrates. He has received the
clinician-scientist and conducts both clinical and basic science highest awards presented by the Canadian Society of Zoologists
research in neonatal hypoxia-reoxygenation injury and neonatal (the Fry Medal), the Comparative and Evolutionary Physiology
transition. Section of the American Physiological Society (the August Krogh
Distinguished Lecture), and the Society for Experimental Biology
Dr Satyan Lakshminrusimha is a neonatologist and the Dennis (UK) (the Bidder Lecture), the three major societies in his disci-
and Nancy Marks Chair and Professor of Pediatrics at the pline. He has also served as the President of the Canadian Society
University of California at Davis, Sacramento, USA. His areas of Zoologists and as President of the International Congress of
of research interest include optimal oxygenation in neonatal Comparative Physiology and Biochemistry. In 2012, Dr Milsom
lung injury, neonatal resuscitation, and pulmonary hyperten- received the Distinguished Service Award from the Canadian
sion. Dr Lakshminrusimha enjoys drawing medical illustra- Society of Zoologists in recognition of contributions to the well-
tions, for which he has developed an international reputation, being of zoology in Canada beyond the call of duty.

ix
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