Eldrin Lewis, MD, MPH New Chief, Cardiovascular Medicine

FALL 2019 Donate to the CVI Eldrin Lewis, MD, MPH new Chief, Cardiovascular Medicine Eldrin Lewis, MD, MPH, has been number of leadership roles, both at Brigham and Women's appointed Professor of Medicine and nationally though the American Heart Association, and Division Chief, Cardiovascular serving as Chair of Heart Failure and Transplant and Vice Chair Medicine, Department of Medicine, of the Council in Clinical Cardiology Leadership Committee. effective March 1, 2020. Dr. Lewis Dr. Lewis is a clinician-scientist who specializes in the care succeeds Drs. Tom Quertermous of patients with advanced heart failure. He has extensive and Alan Yeung who have expertise in conducting clinical trials that examine diagnostic successfully led the division as a and therapeutic approaches to heart failure. He has also done collaborative partnership over the innovative work to create systems that incorporate quality last 20 years. of life measures for cardiovascular patients in electronic Dr. Lewis received his BS at Penn health records. His work has been supported by NIH, private State, his MD from the University of Pennsylvania, and an industry, and foundations, and has been published in top tier MPH from the Harvard School of Public Health. He did his medical and cardiovascular journals. Dr. Lewis also has a long internal medicine residency and fellowships in cardiovascular record of successful mentorship, and has been recognized as medicine and advance heart failure and transplant cardiology an outstanding teacher and mentor. at the Brigham and Women's Hospital in Boston. After, Dr. Dr. Lewis will make an outstanding Professor of Medicine and Lewis joined the faculty of Harvard Medical Center and the Chief of the Division of Cardiovascular Medicine. Brigham and Women's, becoming an Associate Professor https://medicine.stanford.edu/news/current-news/standard-news/ of Medicine in 2015. In addition. Dr. Lewis has served in a Eldrin-Lewis-Cardiology-Chief.html Jayakumar Rajadas, PhD, appointed Assistant Professor of Medicine Jayakumar Rajadas, PhD, was appointed Assistant Professor of Medicine (Pulmonary and Critical Care Medicine and Cardiovascular Research Center) on December 1, 2020. Dr. Rajadas is the Director of Biomaterials and Advanced Drug Delivery Laboratory (BioADD) at Stanford. This center has been involved in bringing biophysical ideas into biomaterial and drug delivery technologies.

Joseph C. Wu, MD, PhD, inducted into the National Academy of Medicine Joseph Wu, MD, PhD, Director of the Stanford Cardiovascular Institute, and Simon H. Stertzer, MD, Professor of Medicine and Radiology, was inducted The 5th annual Stanford Drug Discovery into the National Academy of Medicine (NAM). Symposium features an exciting line-up of Election to the Academy is considered to be one speakers. Save the date for April 21-22, 2020. of the highest honors in the fields of health and Drs. John Schiller and Douglas Lowy will be medicine, recognizing individuals who have demonstrated outstanding presented with the Lifetime Achievement professional achievement and commitment to service. Dr. Wu was elected Award. See page 2 for more details. Registration for his seminal contributions and pioneer breakthroughs in the areas of opens in January. cardiovascular medicine and imaging. https://nam.edu/national-academy-of-medicine-elects-100-new-members/ https://tinyurl.com/SDDS2020 cvi.stanford.edu | 1 Fady Malik, MD, PhD Executive Vice President, R&D Cytokinetics

Mathai Mammen, MD, PhD Global Head of R&D, Janssen Pharmaceutical Company of J&J https://tinyurl.com/sdds2020

PARTICIPANTS INCLUDE: Joan Mannick, MD Elizabeth Blackburn, PhD Co-Founder and CMO Professor Emeritus, UCSF resTORbio Nobel Prize Laureate 2009 Michael Nedelman Stanley Crooke, MD, PhD Producer, Health & Medicine Founder, Chairman, CEO CNN Ionis Pharmaceuticals Menelas Pangalos, FRSB, FMedSci Anthony Fauci, MD Executive Vice President NIAID Director BioPharmaceuticals R&D AstraZeneca William Rutter, PhD Christine Grady, RN, PhD Chairman and CEO Chief of Bioethics, NIH Synergenics

John Schiller, PhD Thomas Hudson, MD Deputy Chief, Laboratory of Cellular CSO Oncology AbbVie National Cancer Institute

Cynthia Kenyon, PhD Lucy Shapiro, PhD Vice President of Aging Research Director, Beckman Center for Molecular Calico and Genetic Medicine Stanford

Paula Kiberstis, PhD Eric Topol, MD Senior Editor Executive Vice President Science Scripps Research Institute

Stephen Knight, MD, MBA Roy Vagelos, MD President and Managing Partner Retired Chairman and CEO, Merck F-Prime Capital Chairman of the Board, Regeneron Pharmaceuticals Dean Li, MD, PhD Wendy Young, PhD Senior Vice President, Discovery Senior Vice President, Small Molecule Sciences and Translational Research Drug Discovery Merck Genentech Douglas Lowy, MD Elias Zerhouni, MD Acting Director Former President for Global R&D, Sanofi National Cancer Institute Former Director, NIH Former US Presidental Science Envoy

Questions: Contact Amanda Chase, PhD, at [email protected]

cvi.stanford.edu | 2 Through Apple Heart Study, Stanford Medicine researchers show wearable technology can help detect atrial fibrillation by Stanford Medicine News Center Wearable technology can safely identify heart rate irregularities that subsequent clinical evaluations confirmed to be atrial fibrillation, reports a study from the Stanford University School of Medicine and Apple now published in the New England Journal of Medicine (NEJM). Atrial fibrillation, a type of irregular heart rhythm, is a leading cause of stroke and hospitalization in the United States, but due to its elusive and often sporadic symptoms, the condition often goes undetected. With more than 400,000 participants enrolled in eight months, the Apple Heart Study is the largest virtual study to date. “The study’s findings will help patients and clinicians understand how devices like Apple Watch can play a role in identifying atrial fibrillation, a deadly and often undiagnosed disease,” said Mintu Turakhia, MD, Associate Professor of Cardiovascular Medicine. “Additionally, these important findings lay the foundation for further research into the Clockwise from top left: Marco Perez, MD; Kenneth Mahaffey, use of emerging wearable technologies in clinical practice and demonstrate the unique potential MD; Manisha Desai, PhD; Mintu of large-scale app-based studies.” Turakhia, MD Turakhia and Manisha Desai, PhD, Professor of Medicine and of Biomedical Data Science, are the senior authors of the study. Marco Perez, MD, associate professor of cardiovascular medicine, is the lead author. The study chair is Kenneth Mahaffey, MD, Professor of Cardiovascular Medicine. The study was launched through a research sponsorship by Apple, Inc., in November 2017 to determine whether software on the Apple Watch could use data from the Watch’s heart-rate pulse sensor to identify atrial fibrillation, which is one of the most commonly diagnosed significant cardiac arrhythmias in the United States, affecting up to 6 million people. During the study, the researchers found that only 0.52% of participants received an irregular pulse notification, assuaging concerns about potential over-notification in healthy participants. Those who were flagged for an irregular pulse received follow-up care through a heart-monitoring technique called an electrocardiography (ECG) patch, which continuously monitors electrical impulses generated by the heart, for one week. Of those who received a notification and were monitored by the ECG patch about two weeks later, 34% were found to have atrial fibrillation. Comparison between irregular pulse-detection on Apple Watch and simultaneous ECG patch recordings showed the pulse detection algorithm has an 84% positive predictive value. During ECG patch monitoring, participants’ Apple Watches continued to monitor pulse irregularities. If a participant had an irregular pulse detected, 84% of the time this was confirmed to be atrial fibrillation on the simultaneous ECG patch. This, said Perez, demonstrates that the algorithm in the Apple Watch can successfully identify atrial fibrillation. Information from this study could be used to inform further clinical evaluation. https://med.stanford.edu/news/all-news/2019/11/through-apple-heart-study--stanford-medicine-researchers-show-we.html

Pressuring the heart to regenerate by Megan Mayerle, PhD The human heart’s structure and function can change in response to stress. Generally, heart muscle cells do not regenerate. However, a team of scientists led by Stanford Cardiovascular Institute member Dr. Ronglih Liao have recently published a paper in the Journal of Molecular and Cellular Cardiology demonstrating that acute increases or decreases in pressure can trigger adult heart muscle cells to proliferate, and that such stimulation could be harnessed therapeutically to promote cardiac repair. The researchers used a reversible surgical technique to increase pressure in the hearts of adult mice, and Ronglih Liao, PhD then after a week, returned pressure to normal in a subset of animals, and then used a molecular labeling technique observe heart cell proliferation. Increasing pressure stimulated cell proliferation, which interestingly was stimulated even further by releasing the pressure. The new cells had all the hallmarks of young heart cells, and tended to be found next to each other, suggesting that proliferation is a localized event. The researchers’ hope is that by understanding how specific stimuli like changes in pressure trigger new heart cell formation, new therapeutic strategies to stimulate/augment natural cardiac regeneration and repair can be developed to help patients. https://med.stanford.edu/cvi/mission/news_center/articles_announcements/pressuring-the-heart-to-regenerate.html cvi.stanford.edu | 3 The final fontier: Studying stem cells on the

International Space Station by Krista Conger Since 2006, iPS cells (short for induced pluripotent stem cells) have been at the forefront of groundbreaking research in biology and medicine. The cells' ability to become nearly any tissue in the body makes them an invaluable resource for physicians wishing to study the effect of drugs on specific, hard-to-obtain tissues or for researchers wanting to delve into the molecular missteps that lead to all manner of diseases.

Now iPS-derived human heart muscle cells called cardiomyocytes have found their way Alexa Wnorowski Arun Sharma, PhD into space, as part of a study by cardiologist and stem cell researcher Joseph Wu, MD, PhD, graduate student Alexa Wnorowski and former Stanford graduate student Arun Sharma, PhD. With the help of NASA astronaut Kate Rubins, PhD, (also a former Stanford graduate student!), Wnorowski and Sharma studied the effect of the low gravity of the International Space Station on the heart cells' structure and function. They published their findings in Stem Cell Reports. Sharma, Wnorowski, and Wu found that the cardiomyocytes cultured on the space station exhibited different patterns of gene expression than did their counterparts grown back here on Earth. They also displayed changes in the way they handled calcium -- an important regulator of contraction rate and strength. Interestingly (and perhaps reassuringly for astronauts like Rubins), the cells appeared to return to normal when their five-and-a-half week jaunt into low Earth orbit ended. "Working with the cells that launched to and returned from the International Space Station was an incredible opportunity," Wnorowski said. "Our study was the first conducted on the station that used human iPS technology, and demonstrated that it is possible to conduct long-term, human cell-based experiments in space." All in all, the researchers were interested to see how nimbly the cells adjusted to their new, free floating life. "We were surprised by how quickly human heart cells adapted to microgravity," Sharma said. "These results parallel known organ-level adaptations that happen to the heart during spaceflight." https://scopeblog.stanford.edu/2019/11/07/the-final-frontier-studying-stem-cells-on-the-international-space-station/

by Amanda Understanding Hypertrophic Cardiomyopathy Chase, PhD Hypertrophic cardiomyopathy (HCM) is a cardiovascular disease characterized by the heart muscle (myocardium) becoming abnormally thick. The thickened heart muscle makes it harder for the heart to pump blood. HCM is usually diagnosed in late adolescence or young adulthood, and is the leading cause of sudden cardiac death in those under age 35. Current treatment is only symptomatic relief, including heart muscle reduction surgery, defibrillator placement, or heart transplant. A new therapeutic approach to treat the disease is urgently needed, but rational drug discovery has been hampered by a lack of understanding of the molecular basis of the disease. Kathleen Ruppel, MD HCM patients display hypercontractility, although the mechanism generating hypercontractility is not understood. It is known that HCM is most often caused by gene mutations, specifically in genes encodingb -cardiac myosin, a motor protein that drives heart muscle contractions. How mutations in the cardiac motor protein leads to altered power output of the protein, thus affecting heart muscle contractility, is not known. Recently, a team of researchers from Stanford University Cardiovascular Institute, led by Kathleen Ruppel, MD, James Spudich, PhD, and first author Arjun Adhikari, PhD, sought to address this question. They generated myosin proteins with four HCM-causing mutations, all known to be clinically pathogenic, and investigated how those HCM-causing mutations alter myosin activity. Their results were recently published in Nature Communications. The researchers were able to show that the specific mutations tested led to an increase in the percentage of myosin motors available to interact with actin; myosin binding to actin results in the power stroke of the myosin motor that drives muscle contraction. Thus, the HCM-causing mutations led to increased cardiac muscle contractility, as seen in HCM patients. Together, the authors were able show that HCM mutations in b-cardiac myosin lead to hypercontractility. These results shed light on a fundamental concept of HCM development, and pushes forward the understanding of the molecular basis of HCM. http://med.stanford.edu/cvi/mission/news_center/articles_announcements/understanding-hypertrophic-cardiomyopathy.html

cvi.stanford.edu | 4 Grants and Awards

Erik Ingelsson, MD, PhD, was awarded an R01 Owais Khan, PhD, received an AHA postdoctoral for "Characterization of novel insulin resistance fellowship. genes by gene editing, high-throughput phenotyping, and in vivo studies".

Alison Marsden, PhD, received an R01 for "Virtual Ke Yuan, PhD, was promoted to Assistant surgery simulator to accelerate medical training Professor of Pediatrics, tenure track, at Boston in cardiovascular disease" and a second R01 Children's Hospital. She was formerly an for "Automated data curation to ensure model Instructor of Medicine - Pulmonary & Critical credibility in vascular model repository". Care Medicine at Stanford.

Michael Ma, MD, received a KL2 Career David Paik, PhD, was promoted to Instructor. Development Award.

Nicholas Leeper, MD, PhD, received the Kevin Moulin, PhD, received an AHA postdoctoral 2019 Special Recognition Award in Vascular fellowship for "Joint diffusion and displacement Biology from AHA and ATVB (Arteriosclerosis, encoded MRI for measuring 'myofiber' strain in Thrombosis and Vascular Biology). diabetic cardiomyopathy".

Sean M. Wu, MD, PhD, received a Sanofi iAward Katharina Schimmel, PhD, received a Vevo Travel grant. Award from VisualSonics for the cardiology track.

Kyle Loh, PhD, was named a Packard Fellow for Tina Baykaner, MD, MPH, was awarded an Science and Engineering. NIH K23 for "Personalizing Atrial Fibrillation Treatment"

Michelle Kaplinski, MD, received a Maternal & Myriam Amsallem, MD, PhD, was appointed Child Health Research Institute (MCHRI) Clinical Instructor in the Department of Cardiovascular Education Grant. Medicine

Joseph Woo, MD, received the Surgery Mentoring Jennifer Attam Arthur, PhD, received an AHA Award from the Council on Cardiovascular postdoctoral fellowship award Surgery and Anesthesia (CVSA).

Donate to the Stanford Cardiovascular Institute The Institute currently consists of over 240 faculty members representing physicians, surgeons, engineers, basic and clinical researchers. The Institute's mission is integrating fundamental research across disciplines and applying technology to prevent and treat cardiovascular disease. To support cardiovascular research and education at CVI, please contact: Joseph C. Wu, MD, PhD, CVI Director at [email protected] or Cathy Hutton, Senior Associate Director, Medical Center Development at [email protected]. Joseph C. Wu, Cathy Hutton, MBA For more: http://med.stanford.edu/cvi/support-our-research.html and http://cvi.stanford.edu MD, PhD

cvi.stanford.edu | 5 CVI hosts Stanford - UPenn Cardiovascular Research Symposium in November The Stanford-Penn Cardiovascular Symposium was held over two days, November 4-5, 2019, highlighting ongoing cardiovascular research at both institutions. The symposium was attended by over 300 people, from basic scientists to industry representatives to clinicians. The conference was hosted by the Stanford Cardiovascular Institute, in conjunction with the University of Pennsylvania Cardiovascular Institute, with the mission of fostering productive collaborations. The event opened with a keynote address by Peter Fitzgerald, MD, PhD, Professor Emeritus of Cardiovascular Medicine and Medicine & Engineering, who spoke about “Future in Health: Drugs, Devices, and Data”. The second day kicked off with a keynote address by Daniel Rader, MD, Seymour Gray Professor of Molecular Medicine at the University of Pennsylvania, entitled: “A Genome-Frist Approach to Cardiometabolic Disease”. In addition, twenty- four Stanford and Penn cardiovascular researchers presented their research, and there were eleven rapid fire talks from junior scientists. The conference ended with an engaging poster session, where over forty posters were presented and discussed. We look forward next year's CVI Retreat, a joint conference with Cornell University on October 15-16. Recruitment for T32 Fellowships Multi-Disciplinary Training Program in Cardiovascular Imaging T32 Training Grant The Multi-Disciplinary Training Program in Cardiovascular Imaging at Stanford is funded by the National Institute of Biomedical Imaging and Bioengineering of the National Institutes of Health. With the impact of cardiovascular disease on U.S. and world health, and the rapid advances in imaging technologies and cardiovascular biology, it is critical that fellows be provided a broad, multi-disciplinary, and collaborative training program to foster their ability to translate CV imaging research into clinical applications. The program is designed to train the next generation of CV imaging investigators by exposing them to three complementary areas—clinical, engineering, and molecular imaging. http://med.stanford.edu/cvi/education/cardiovascular-imaging-t32.html Mechanisms and Innovations in Cardiovascular Disease T32 Training Grant This program provides training in the following areas of vascular medicine and research: Vascular Reactivity and Thrombosis, Vascular Regeneration and Development, Metabolic or Lifestyle Influences on Vascular Outcomes, Proteomic Markers & Genetic Determinants of Vascular Disease, Gender and Ethnicity Differences in Vascular Disease, and Vascular Bioengineering. Twenty-nine faculty mentors from eighteen different departments within the School of Medicine and the University provide a variety of angles from which to address fundamental questions about vascular disease. http://med.stanford.edu/cvi/education/mechanisms-and-innovations-t32.html Research Training in Myocardial Biology T32 Training Grant - 2 Openings The Multi-Disciplinary Research Training Program in Myocardial Biology is funded by the National Institutes of Health to bring together post-doctoral fellows and faculty from six complementary areas – genetics and genomics, cellular signaling, molecular imaging, physiology and phenotyping, cardiac development and regeneration and outcomes research and population science. Although many possible divisions exist in the spectrum of cardiovascular investigators, one of the most discrete is the division between those researchers interested in blood vessels and those primarily interested in the biology of the heart muscle itself. Myocardial biologists at Stanford are found in diverse departments and divisions within the wider Stanford community and this provides a natural vehicle for multidisciplinary training. http://med.stanford.edu/cvmedicine/education/timbs.html cvi.stanford.edu | 6 Tools to understand heart contraction by Amanda Chase, PhD The heart enables blood to be pumped throughout the body. This is done through a series of coordinated signaling that stimulates muscle contractions, and is coordinated by the cardiac conduction system. The cardiac conduction system (CCS) is made up of a group of specialized cardiac muscle cells that each carry out a particular task to establish the coordinated contractions and the rhythmic beating of the heart. The CCS is essential for normal function of the heart. Dysfunction in the CCS causes irregular, fast, or slow heart rhythms, and severe cases can result in arrhythmias, decreased cardiac output, or sudden Sean Wu, MD, PhD William Goodyer, MD, PhD death. The CCS is composed of several unique cardiac cells, each with their own physiological and electrochemical properties. However, there is currently limited knowledge on the distinct CCS cell types, which would allow a better understanding of the cellular and molecular landscape that facilitates heart development and function. Recently, a group of researchers with the Stanford Cardiovascular Institute, led by William Goodyer, MD, PhD, and senior author Sean Wu, MD, PhD, addressed this gap in knowledge by leveraging single-cell RNA sequencing to understand global gene expression analysis at a single-cell resolution. The work was recently published in Circulation Research. Single-cell RNA sequencing (scRNA-seq) provides a higher resolution of cellular differences to provide a better understanding of the function of an individual cell. In this paper, the authors performed scRNA-seq on over twenty thousand cells from heart tissues enriched for CCS cells in developing mouse hearts to successfully capture all components of the CCS, including cell types that were previously unattainable. They were also able to discover a unique set of genes expressed in the CCS, as well as various cell subtypes, and were able to uncover several novel markers and unique molecular signatures of various cell subtypes to provide a molecular blueprint of the CCS. This study provided the first look at the entire CCS at the single-cell level, which has important implications for understanding CCS's role in heart development and function. Furthermore, the authors provide a tool to facilitate future efforts to isolate and characterize cells in the context of development and disease. Together, the information and tools derived from this work will improve our ability to diagnose and treat diseases of the CCS (i.e., arrhythmias) in utero and during adulthood. http://med.stanford.edu/cvi/mission/news_center/articles_announcements/tools-to-understand-heart-contraction.html

ENLIGHTEN-ing a population by Damon Williams In a paper recently published in the Journal of Community Health, a team of researchers outlined the effectiveness of a monthly lifestyle education program on increasing the cardiovascular health of pre- hypertensive adults in a low-income urban setting. This study was led by first author Julieta Gabilola, MD, clinical professor of medicine at Stanford and senior author Latha Palaniappan, MD, MS, professor of medicine at Stanford. The ENLIGHTEN study (the EffeciveNess of LIfestyle with diet and physical education proGram among Latha Palaniappan, prehypertensives and stage 1 HyperTENsives in an urban community setting) is an intervention study MD, MS that compares select health metrics of a group of individuals that was assigned to either an intervention or attention-control group. The intervention group was exposed to lectures on cardiovascular disease, as well as organized lectures on diet and exercise. The attention-control group, however, only received lectures on non-cardiovascular topics, only receiving the advice that a healthy diet and exercise are important. The aim was to determine if educational programs alone could be used as a resource for improving hypertension levels and, ultimately, cardiovascular health. To test their question, the researchers had 156 participants in Manila, Philippines, who were assigned to either the attention- control group or the intervention group, and who participated for the full 6 months. The primary outcome for the study was looking for blood pressure reduction, with secondary outcomes including waist circumference, total cholesterol, and fasting glucose, all measures associated with cardiovascular health. The researchers found that the monthly education sessions (intervention group) had profound positive effects on the health of the selected individuals. They noticed a statistically significant decrease in systolic blood pressure, BMI, waist circumference, total cholesterol, and glucose levels. Importantly, these findings show the feasibility of implementing lifestyle interventions and education programs in the Philippines and other developing countries with limited health care resources in improving cardiovascular health. http://med.stanford.edu/cvi/mission/news_center/articles_announcements/enlighten-ing-a-population.html cvi.stanford.edu | 7 CVI Seed Grants 2019-2020 (FY 2020) The Stanford Cardiovascular Institute has provided over $2.7 million in seed funding to support research in cardiovascular research and innovation since 2004. Our goal is to ignite and support new ideas that will change how we diagnosis and treat cardiovascular diseases. Together with Stanford Maternal and Children's Health Research Institute (MCHRI) and the Gootter Foundation, the CVI is excited to support research for 11 outstanding projects in 2020. Seed Grants funded by the Maternal & Child Health Research Institute PIs: Francois Haddad, MD; Myriam Amsallem, MD, PhD; Jeffrey Feinstein, MD, MPH Co-Investigators: Alison Marsden, PhD; Roham T. Samanian, MD; David Ouyang, MD Developing Novel Computational Methods for the Early Detection of Right Heart Failure and Pulmonary Hypertension in the Pediatric and Adult Populations PI: Sushma Reddy, MD Co-Investigators: Daniel Bernstein, MD; Jingjing Li, PhD A Non-invasive Signature of Myocardial Signaling in Children with Single Ventricle Heart Failure

PIs: Ioannis Karakikes, MD; Kevin Wang, MD, PhD CRISPR-mediated Therapy for Cardiac Laminopathies

PIs: Nicholas Leeper, MD; Ying Wang, PhD Identify 'Atherogenic' Somatic Mutations/Epigenetic Modifications in Vascular Smooth Muscle Cells

PIs: David Paik, PhD; Kari Nadeau, MD, PhD Co-Investigator: Lei Tian, PhD Single-cell Sequencing to Identify Air Pollution-Induced Cardiac Risks

PI: Marlene Rabinovitch, MD Co-Investigators: Michael Snyder, PhD; David Marciano, PhD; Jan-Renier Moonen, MD, PhD Exploring Genomic Mosaicism in Pulmonary Arterial Hypertension Patient Lungs

PI: Elsie Ross, MD Co-Investigators: Nigam Shah, MBBS, PhD; Nicholas Leeper, MD; Erik Ingelsson, MD, PhD; Philip Tsao, PhD Development of a Precision Screening Platform for Peripheral Artery Disease Using Electronic Health Records and Polygenic Risk Scores PIs: Jennifer Tremmel, MD; Patricia Nguyen, MD Co-Investigators: Vedant Pargaonkar, MD; Thomas Quertermous, MD Whole Exome Sequencing Study of Coronary Microvascular Dysfunction in Patients with Angina in the Absence of Obstructive Coronary Arter Disease

PIs: Ronald Witteles, MD; Euan Ashley, MRCP, PhD; Kevin Alexander, MD Co-Investigators: Francois Haddad, MD; Paul Cheng, MD, PhD; David Ouyang, MD Precision Approach to Ventricular Mass: Image-Based Differentiation of Hypertrophic Cardiomyotaphy, Amyloidosis, and Phenocopies

PI: Phillip Yang, MD Co-Investigators: Utkan Demirci, PhD; Katrin Svensson, PhD Proteomic Analysis of iPSC-derived Extracellular Vesicles for Mitochondrial Biogenesis

Seed Grant Funded by the Steven M. Gootter Foundation PI: Paul Wang, MD Co-Investigators: Duy Nguyen, MD; Anson Lee, MD; Mohan Viswanathan, MD; Nitish Badhwar, MD; Sanjiv Narayan, MD; Oscar Abilez, MD, PhD; Phillip Yang, MD; Meghedi Babakhanian, PhD; Terrance Pong, MD; Paul Chang, MD Experimental Heart Models of Ventricular Tachycardia: Porcine and Explanted Human Heart cvi.stanford.edu | 8 A method to shed light on the genetic underpinnings of complex human traits by Megan Mayerle, PhD Human genetic studies have been highly instrumental in ushering in the current precision medicine era. Such initiatives have been profoundly successful at identifying genomic regions that cause or contribute to many diseases. However, there have been significant challenges in actually using such information to treat patients. Such challenges are often due to pleiotropy, or when one gene can have multiple, disparate effects, and to the fact that many complex diseases do not have simple underlying genetic causes, and instead arise from a constellation of genetic and environmental factors. Erik Ingelsson, MD, In an article published in Nature Communications, a team of researchers led by CVI member Dr. Erik Ingelsson PhD and Dr. Manuel Rivas has developed and applied a new methodology to address this problem. Building on a mathematical technique known as Singular Value Decomposition, the authors developed DeGAs, or decomposition of genetic associations, and a freely available web app for using their methodology. The technique allows researchers to combine information from a wide variety of sources while preserving data interpretability. Next, using data from the UK Biobank, the researchers applied DeGAs to try to understand body mass index (BMI), myocardial infarction (MI), and gallstones, all of which are complex human traits and diseases that can arise from a complex combination of genetic and environmental factors. The researchers identified loss-of-function variants in two genes that contribute to obesity, and followed that up with functional experiments in adipocytes to demonstrate a role for these genes in fat cell differentiation, presumably underlying their role in obesity development. DeGAs provides a starting point that enables scientists to investigate genetic components, their functional relevance, and potential therapeutic targets and is an approach that can be applied to a wide variety of human diseases. https://med.stanford.edu/cvi/mission/news_center/articles_announcements/a-method-to-shed-light-on-the-genetic-underpinnings-of-complex-h.html 2019 AHA Scientific Sessions The 2019 AHA Scientific Sessions was held November 16-18 in Philadelphia, Pennsylvania. This annual meeting brings together basic, translational, and clinican scientists and physicans to discuss and present innovative findings. Stanford CVI was well represented, with fellows, faculty, and staff in attendence. Several presented posters or concurrent session presentations. Dr. Robert Harrington, Chair of the Department of Medicine and AHA president, presented the Presidental Address. He spoke about the exciting time it is to be in cardiovascular health, and in science, and that evidence matters in all aspects of treating CV disease and should be the basis for decision making.

Michael Fischbein, MD, moderated a AHA President, and Chair Ngan Huang, PhD, spoke on biomaterials for series of debates of Department of Medicine endothelial to mesenchymal transition for vascular Joseph Woo, MD, presented two regarding the optimal at Stanford, Robert regeneration. She also moderated a session and her talks on the commando procedure treatment plans for Harrington, MD, giving the group presented 2 posters as well as intraoperative tips on difficult cases. Presidential Address. ventricular rupture after mitral surgery. His group presented 5 posters. Dr. Woo also received the Surgery Mentoring Award from the council of Cardiovascular Surgery and Anesthesia (CVSA)

Faddy Grady with Dr. Joseph Wu. Faddy was awarded the Minority Travel Grants from the Council on Drs. Joseph Wu and Finalists for the Louis N. and Arnold Basic Cardiovascuar Science. Ronglih Liao M. Katz Basic Research Prize for Early Career Investigators cvi.stanford.edu | 9 Inflammation may trigger silent mutation causing sudden onset of pulmonary hypertension by Tracie White Researchers at the Stanford University School of Medicine have found that inflammation in the lungs of rats, triggered by something as simple as the flu, may wake up a silent genetic defect that causes sudden onset cases of pulmonary hypertension, a deadly form of high blood pressure in the lungs. “It’s a kind of one-two punch,” said Amy Tian, PhD, senior research scientist in pulmonary and critical care. “Basically, the first hit is the mutation, and the second hit is inflammation in the arteries of the lungs. You can be healthy and carrying this mutation, and all of the sudden you get a bacterial or viral infection, and Mark Nicolls, MD it leads to this terrible disease. ” Tian is the lead author of the study, which was published Aug. 29 in Circulation. Mark Nicolls, MD, Professor and Chief of Pulmonary and Critical Care Medicine, is the senior author. There is no known cause of pulmonary hypertension, a debilitating disease that causes difficulty breathing, fatigue and chest pain. It can leave patients too weakened to perform simple daily activities, such as climbing a flight of stairs. About 200,000 people a year are hospitalized with the disease in the United States, Amy Tian, PhD according to the Pulmonary Hypertension Association of America. The only available cure for severe forms of the disease is lung transplantation, but it has only a 30% survival rate. Treatment is limited to vasodilators, drugs that cause the smooth muscle cells of the diseased blood vessels in the lungs to relax, permitting more blood to flow through. These drugs help to extend survival and relieve some symptoms, but they are not a cure. Thus, scientists have been searching for other therapies. Past research has shown that the majority of patients with the inherited form of pulmonary hypertension, which is also the most lethal, carry a mutation in the gene BMPR2. Whether the mutation plays a role in causing the disease has been unclear. Surprisingly, 80% of people with the mutation don’t get the disease and remain perfectly healthy, Nicolls said. Based on previous research into inflammation in the lungs, the Stanford researchers hypothesized that an inflammation- producing pathway may provide the second “hit” that triggers the mutation to cause the disease in certain patients. Based on previous research into inflammation in the lungs, the Stanford researchers hypothesized that an inflammation-producing pathway may provide the second “hit” that triggers the mutation to cause the disease in certain patients. Indeed, their results indicate that limiting potential environmental causes of lung inflammation in patients with a genetic risk for pulmonary hypertension may help prevent the development of the disease. https://med.stanford.edu/news/all-news/2019/08/inflammation-triggers-silent-mutation-to-cause-deadly-lung-disease.html

Unconscious bias: The double-edged sword by Damon Williams In her recent publication in the Thoracic Surgery Clinics Journal, Associate Professor of Cardiothoracic Surgery Dr. Leah Backhus comprehensively explores the complex topic of unconscious bias (UB) and discusses the positive and negative effects that it has on surgical education with a spotlight on cardiothoracic surgery. She details how the “hidden brain” can be beneficial by hastening decision-making in time-sensitive situations, such as during a thoracic surgery operation. However, it can also have negative effects on trainees, such as contributing to feelings of alienation, negatively impacting their performance, damaging their mental health, and at times playing a role in which specialty they choose or how well they excel in their chosen Leah Backhus, MD field. These effects are especially prevalent in female and African American surgical trainees. Backhus provides striking statistics from the American Board of Surgery In-Training Examination surveys showing that African American surgical residents are less likely to believe they can count on their peers for help. Other survey data report that male surgical trainees have a 12.7% higher rate of milestone attainment throughout residency programs compared to their female counterparts. Importantly, this is in spite of evidence demonstrating equal surgical board pass rates. As the medical (and pre-medical) education student body continues to become more diverse and inclusive to individuals of all backgrounds, it is important to shed light on these issues with the added (and equally important) benefits towards reducing disparities in healthcare delivery and health outcomes for our patients. Dr. Backhus is helping leading medical education in the right direction by both addressing and providing solutions to these issues in a healthy and positive way. http://med.stanford.edu/cvi/mission/news_center/articles_announcements/unconscious-bias--the-double-edged-sword.html cvi.stanford.edu | 10 Frontiers in Cardiovascular Sciences Seminar Lineup Javid Moslehi, MD Yibin Wang, PhD Anthony Rosenzweig, MD Vanderbilt University UCLA School of Medicine Harvard Medical School January 7, 2020 January 14, 2020 January 21, 2020

Sharlene Day, MD Martin Pera, PhD Geoffrey Ginsburg, MD, PhD UPenn Jackson Laboratory Duke University January 28, 2020 February 4, 2020 February 11, 2020

Manuela Zaccolo, MD, PhD Cornelia Weyand, MD, PhD Maria Kontaridis, PhD Oxford Stanford University Masonic Medical Research February 18, 2020 February 25, 2020 Institute March 3, 2020 Join us Tuesday afternoons to hear the latest in Cardiovascular and Pulmonary Research. Exact times and locations available at https://med.stanford.edu/cvi/mission/frontiers-in-cv-science.html The science and art of grant writing As you sit down to write a grant proposal, remember one thing — you’re telling a story. You want it to be a page-turner. Your primary audience will be a few busy senior scientists sitting in front of a tall stack of applications. You should strive to make yours interesting. The specific aims page should spark their curiosity. A new solution to an old problem. Connections that have never been made before. Then you’ll get your grant. This was the main message delivered at a half-day grant Biosciences Grant Writing writing symposium held on July 25, organized by Stanford’s Biosciences Grant Writing Academy. Academy half-day symposium “The Science and Art Grant Writing Symposium” featured 11 distinguished Stanford scientists, all experienced grant writers and reviewers, who offered up their collective wisdom on how to write an amazing proposal. Stanford has a wealth of resources to hone your grant writing sktills. These include articles, online courses, hands-on assistance, and video tutorials. https://med.stanford.edu/researchofficebulletin/topics/The-science-and-art-of-grant-writing.html MED223 | Cardiopulmonary Research & Medicine The focus of MED223 is to fine-tune critical thinking skills by analyzing original publications and understanding the current complexities of the cardiovascular system. MED223 is part of the Scholarly Concentration: Cardiovascular-Pulmonary Sciences. For more information, contact MED223 Directors: Ngan Huang, PhD, Ioannis Karakikes, PhD, Edda Spiekerkoetter, MD, and Vinicio de Jesus Perez, MD. MED223 website: https://med.stanford.edu/cvi/education/cvi-courses/med223.html

Francois Haddad, MD Kevin Alexander, MD Andrew Sweatt, MD Oscar Abilez, MD, PhD TBA January 9, 2020 January 16, 2020 January 23, 2020 January 30, 2020 February 6, 2020

June Rhee, MD Natalie Lui, MD Jonathan Myers, PhD Amy Tian, PhD Marlene Rabinovitch, MD February 13, 2020 February 20, 2020 February 27, 2020 March 5, 2020 March 12, 2020

cvi.stanford.edu | 11 Funding Opportunities

DECEMBER 2019 NIH Exploratory/Developmental Research Grant Program (Parent R21 Clinical Trial Not Allowed). Due Date: February 16, 2020, PA-19-053 Ruth L. Kirschstein National Research Service Award (NRSA) Individual Postdoctoral Fellowship. (Parent F32) Postdocs. New NIH Exploratory/Developmental Research Grant Program (Parent application deadline: Dec 8, 2019. PA-19-188 R21 Clinical Trial Required). Due Date: February 16, 2020. PA-19-054 NIDDK Small Grants for New Investigators to Promote Diversity in Health-Related Research (R21 Clinical Trial Optional). Due Date: JANUARY 2020 February 16, 2020. PAR-19-222 American Heart Association. End the Lies: Youth Vaping and Nicotine Research Initiative. Deadline: Tues, Jan. 7, 2020 MARCH 2020 ISHLT/Enduring Hearts Transplant Longevity Research Award. Tobacco-Related Disease Research Program of California (TRDRP) Deadline: January 13, 2020 Community-Partnered Participatory Research Award. Stanford PI ISHLT/O.H. Frazier Award in MCS Translational Research (Sponsored Eligibility: Faculty with PI eligibility and CE faculty (with an approved CE by Medtronic). For junior faculty dedicated to a career in the use Faculty PI waiver obtained 1-2 weeks prior to the LOI submission). Full of MCS as a treatment option for heart failure. Deadline: January application: March 5, 2020 13, 2020 NIH Research Project Grant (Parent R01 Clinical Trial Not Allowed). Renewal, Revision, Resubmission Deadline: March 5, 2020. PA-19-056 American Heart Association. Increasing Awareness and Action for the Prevention of Cardiovascular Disease and Cerebrovascular Disease in NIH Research Project Grant (Parent R01 Clinical Trial Required). Millennial Women within Underrepresented Ethnic and Racial Groups Renewal, Revision, Resubmission Deadline: March 5, 2020. PA-19-055 Deadline: Wed., Jan. 15, 2020 NIH Pathway to Independence Award (Parent K99/R00 - Independent 2020 Stanford Clinical and Translational Science Award (CTSA) Clinical Trial Required). Renewal, Revision, Resubmission Deadline: SPADA Pilot Grants: Request for Proposals. Application Due: Friday, March 12, 2020. PA-19-129 January 10, 2020 at 6 pm NIH Pathway to Independence Award (Parent K99/R00 Independent American Heart Association 2020 Transformational Project Award. Basic Experimental Studies with Humans Required). Renewal, Deadline: Wed., Jan. 22, 2020 Revision, Resubmission Deadline: March 12, 2020. PA-19-090 Tobacco-Related Disease Research Program of California (TRDRP) NIH Mentored Patient-Oriented Research Career Development Award Rapid Response Research to Accelerate Policy Award. Stanford PI (Parent K23 Independent Clinical Trial Required). Renewal, Revision, Eligibility: Faculty with PI eligibility and CE faculty (with an approved CE Resubmission Deadline: March 12, 2020. PA-19-118 Faculty PI waiver obtained 1-2 weeks prior to the LOI submission). Full NIH Mentored Patient-Oriented Research Career Development Award application: January 23, 2020 (Parent K23 – Independent Clinical Trial Not Allowed). Renewal, Stanford Seed Funding CARE Seed Grant. (Sponsored by Center for Revision, Resubmission Deadline: March 12, 2020. PA-19-119 Asian Health Research and Education) Deadline: January 27, 2020 NIH Mentored Clinical Scientist Research Career Development NHLBI Program Project Applications (P01 -Clinical Trial Optional). Award (Parent K08 Independent Clinical Trial Not Allowed). Renewal, The proposed programs may address scientific areas relevant to the Revision, Resubmission Deadline: March 12, 2020. PA-19-117 NHLBI mission including the biology and diseases of the heart, blood NIH Mentored Clinical Scientist Research Career Development Award vessels, lung, and blood; blood resources; and sleep disorders. Due Date: (Parent K08 Independent Clinical Trial Required). Renewal, Revision, January 25, 2020 Resubmission Deadline: March 12, 2020. PA-19-116 NHLBI T32 Training Program for Institutions That Promote Diversity NIH Exploratory/Developmental Research Grant Program (Parent (T32 – Clinical Trial Not Allowed). Due Date: January 25, 2020 R21 Clinical Trial Not Allowed). Renewal/Revision Due Date: March 16, 2020.PA-19-053

FEBRUARY 2020 NIH Exploratory/Developmental Research Grant Program (Parent R21 Clinical Trial Required). Renewal/Revision Due Date: March 16, NIH Research Project Grant (Parent R01 Clinical Trial Not Allowed). 2020. PA-19-054 New application Deadline: February 5, 2020. PA-19-056 NIH Research Project Grant (Parent R01 Clinical Trial Required). New application Deadline: February 5, 2020. PA-19-055 ROLLING DEADLINE NIH Single-Site Investigator-Initiated Clinical Trials (R61/R33 Mackay California-Pacific Rim Tobacco Policy Scholar Award. $250K/yr Clinical Trial Required) Deadline: February 11, 2020. PAR-19-328 x 3 yrs. Build leadership among mid-career researchers to foster evidence- based tobacco control policy with relevance to California and the Pacific NIH Mentored Career Development Award to Promote Faculty Rim (Asia, Pacific Islands and Latin America). Eligibility: mid-career faculty Diversity in Biomedical Research (K01 Independent Clinical Trial with PI eligibility and mid-career CE faculty (with an approved CE faculty Required). Deadline: February 12, 2020. RFA-HL-19-025 PI waiver >>). Applicants must be 5 years post completion of his/her NIH Mentored Career Development Award to Promote Faculty terminal degree or 5 years post-completion of his/her medical residency Diversity in Biomedical Research (K01 Independent Clinical Trial Not at the start of the award. Note: Stanford visiting scholars are not eligible to Allowed). Deadline: February 12, 2020. RFA-HL-19-026 be PIs. Awardees are required to commit at least 35% of their effort each year. No citizenship requirement NHLBI Outstanding Investigator Award (OIA) (R35 Clinical Trial Optional). Due Date: February 14, 2020. RFA-HL-20-011

cvi.stanford.edu | 12 National and Global Cardiovascular Conferences

JANUARY 2020 MARCH 2020

Mayo Clinic Cardiology Update at Puerto Vallarta: A Focus on Mayo Clinic Ski the Summit @ Copper: Echo Imaging in Prevention. January 6-10, 2020. Marriott CasaMagna, Puerto Colorado. March 1-5, 2020. Copper Mountain Resort, Copper Vallarta, Mexico Mountain, CO, USA

Mayo Clinic Hawaii Echo with Multimodality Imaging. January Keystone Symposia New Insights into the Biology of Exercise 18-23, 2020. Ritz Carlton Kapalua, Kapalua, Maui, HI (Q7). March 1-5, 2020. Keystone Resort, Keystone, CO, USA

Keystone Symposia Hypoxia: Molecules, Mechanisms and Keystone Symposia Charting a New Course for Heart Failure: Disease (A3). January 19-23, 2020. Keystone Resort, Keystone, From Discovery to Data (Q8). March 1-5, 2020. Keystone Resort, CO, USA Keystone, CO, USA

Keystone Symposia Beyond a Million Genomes: From American Heart Association EPI|LIFESTYLE 2020 Scientific Discovery to Precision Health (A4). January 21-25, 2020. Beaver Sessions. Epidemiology and Prevention | Lifestyle and Run Resort, Breckenridge, CO, USA Cardiometabolic Health. March 3–6, 2020. Hyatt Regency Phoenix. Phoenix, AZ, USA Mayo Clinic Arrhythmias and the Heart: A Cardiovascular Update. January 27-31, 2020. Fairmont Orchid, Kohala Coast, Mayo Clinic Cardiac Rehabilitation Workshop: The Mayo HI, USA Clinic Model. March 24-26, 2020. Rochester, MN, USA

Vascular & Endovascular Surgery Society. January 30- The American College of Cardiology's 69th Annual Scientific February 2, 2020. 2020 Annual Winter Meeting. Steamboat Session & Expo. March 28–30, 2020. Chicago, Illinois, USA Grand, Steamboat Springs, CO, USA Mayo Clinic Heart Failure Management for NP, PA, and Primary Care Providers. March 26-28, 2020. Disney's Grand Floridian Resort. Lake Buena Vista, FL, USA FEBRUARY 2020 Mayo Clinic Extracorporeal Membrane Oxygenation (ECMO) Keystone Symposia Antibodies as Drugs: From B Cell Biology Symposium 2020. March 27-28, 2020. Scottsdale, AZ USA to New Treatments (B1). February 2-6, 2020. Eldorado Hotel & Spa, Santa Fe, NM, USA

Mayo Clinic Cardiovascular Conference at Snowbird. February 5-8, 2020. Cliff Lodge, Snowbird, UT, USA

Mayo Clinic Cardio-Oncology: Practical Strategies to Advance Your Practice 2020. February 13-15, 2020. Scottsdale, AZ, USA

American Heart Association International Stroke Conference 2020. Precon & Nursing: Feb. 18 | Sessions: Feb. 19–21, 2020 | Los Angeles, CA, USA

Keystone Symposia Cerebral Fluid Flow and Function: Lymphatics, Glymphatics and the Choroid Plexus (Q4). February 16-19, 2020. Eldorado Hotel & Spa, Santa Fe, NM, USA

Keystone Symposia Fibrosis and Tissue Repair: From Molecules and Mechanics to Therapeutic Approaches (Q6). February 19-23, 2020. Fairmont Empress Victoria, Victoria, BC, Canada

Mayo Clinic. Cardiology at Cancun: Topics in Clinical Cardiology. February 24-28, 2020. Marriott Cancun Resort, Cancun, Mexico

cvi.stanford.edu | 13 CVI Cores Stanford CVI Human iPSC Biobank Service Normal and patient-derived reprogrammed cardiomyocytes are a tremendous resource for researchers and physicians here at Stanford and around the country. Understanding the disease process directly at the population level and observing these cells as Cardiovascular surrogates under a myriad conditions has the potential to be a game-changer for cardiovascular medical research. Pharmacology (BioADD)

To facilitate research in a dish that allows screening of new compounds or characterization of The Cardiovascular Pharmacology/ human disease phenotypes using cardiomyocytes, the Institute created a service by which Biomaterials and Advanced Drug Delivery de-identified peripheral blood mononuclear cell (PBMC) samples from selected patients (BioADD) Laboratory is a cutting edge can be sent to Stanford CVI for reprogramming free of cost. research facility that specializes in the creation of biomaterials and drug delivery SCVI biobank is supported in part by National Heart, Lung and Blood Institute (NHLBI) and the agents. The lab lends its expertise toward Stanford Cardiovascular Institute (CVI). designing and analyzing biomaterials, developing drug delivery devices and Contact: Joseph Wu, MD, PhD / [email protected] formulations, pharmacokinetic and or Biobank manager, Yan Zhuge, PhD / [email protected] with any questions. pharmacodynamic studies, and developing smart materials for biomedical applications. The CVI Cardiovascular Pharmacology also offers trainings and lectures. Clinical Biomarker & Phenotyping Core Lab (BPCL)

BPCL provides quantitative assessment of clinical cardiovascular Contact: Jayakumar Rajadas, PhD phenotypes for translational research and clinical trials. These [email protected] cardiovascular phenotypes include evaluating cardiac structure and function, measuring carotid intimal thickness and arterial stiffness, and testing endothelial function and cardiopulmonary exercise testing.

In collaboration with the Human Immune Monitoring Center at Stanford and members of the Cardiovascular Institute, we also offer central blood processing and banking capabilities. In addition, we develop new biomarker platforms and imaging modalities. Contact: Francois Haddad, MD / [email protected] 3DQ Imaging Laboratory

Stanford’s 3DQ Imaging Laboratory CVI Clinical Trials Core develops new approaches to exploration, analysis and quantitative assessments The CVI Clinical Trials Core provides full spectrum of support to CVI members and their clinical of diagnostic images that result in new trials. The coordinators has extensive clinical research experience in both industry and academia. and/or more cost-effective diagnostic The team provides services and support to principal investigators and sponsors, including: approaches, and new techniques for the design and monitoring of therapy. The • Consultation • Data management lab processes over 1,200 clinical cases to • Study start-up management, including • Regulatory compliance and documen- deliver relevant visualization and analysis IRB applications, budget development tation of medical imaging data at Stanford. The • Subject recruitment, site visits, and • Closeout lab is co-directed by Dominik Fleischmann, follow-ups (AE reporting and queries) MD, Roland Bammer, PhD and Sandy Napel,

PhD. Contact: Ed Finn, Clinical Trials Manager at [email protected] Contact: Dominik Fleischmann, MD / [email protected]

cvi.stanford.edu | 14 Member Publications

Communication is at the heart of scientific advancement and innovation. This quarter, the Stanford Cardiovascular Institute members published over 350 original manuscripts and reviews, further contributing to our understanding of cardiovascular biology and disease. Here, we highlight selected manuscripts by our members.

A preclinical model links osseo-densification due to misfit and osseo- SEPTEMBER destruction due to stress/strain. Coyac BR, Leahy B, Salvi G, Hoffmann W, Brunski JB, Helms JA. Clin Oral Implants Res. 2019 Sep 14. doi: 10.1111/clr.13537. Workload-indexed blood pressure response is superior to peak systolic Association Between Current and Future Annual Hospital Percutaneous blood pressure in predicting all-cause mortality. Hedman K, Cauwenberghs Coronary Intervention Mortality Rates. Sandhu AT, Kohsaka S, Bhattacharya J, N, Christle JW, Kuznetsova T, Haddad F, Myers J. Eur J Prev Cardiol. 2019 Sep Fearon WF, Harrington RA, Heidenreich PA. JAMA Cardiol. 2019 Sep 18:1-8. doi: 30:2047487319877268. doi: 10.1177/2047487319877268. 10.1001/jamacardio.2019.3221. The GABA receptor GABRR1 is expressed on and functional in hematopoietic Pathological overlap of Arrhythmogenic Right Ventricular Cardiomyopathy stem cells and megakaryocyte progenitors. Zhu F, Feng M, Sinha R, Murphy MP, and Cardiac Sarcoidosis. Kerkar A, Hazard F, Caleshu CA, Shah RL, Reuter Luo F, Kao KS, Szade K, Seita J, Weissman IL. Proc Natl Acad Sci U S A. 2019 Sep C, Ashley EA, Parikh VN. Circ Genom Precis Med. 2019 Sep 21. doi: 10.1161/ 10;116(37):18416-18422. doi: 10.1073/pnas.1906251116. CIRCGEN.119.002638. Beyond duty hours: leveraging large-scale paging data to monitor resident Beyond the Lungs: Systemic Manifestations of Pulmonary Arterial workload. Kaushal A, Katznelson L, Harrington RA. NPJ Digit Med. 2019 Sep Hypertension. Nickel NP, Yuan K, Dorfmuller P, Provencher S, Lai YC, Bonnet S, 9;2:87. doi: 10.1038/s41746-019-0165-2. eCollection 2019. Austin ED, Koch CD, Morris A, Perros F, Montani D, Zamanian RT, de Jesus Perez Automated Detection of Intracranial Large Vessel Occlusions on Computed Am J Respir Crit Care Med. 2019 Sep 12. doi: 10.1164/rccm.201903-0656CI. VA. Tomography Angiography: A Single Center Experience. Amukotuwa SA, Straka The DNA Repair Nuclease MRE11A Functions as a Mitochondrial Protector and M, Smith H, Chandra RV, Dehkharghani S, Fischbein NJ, Bammer R. Stroke. 2019 Prevents T Cell Pyroptosis and Tissue Inflammation. Li Y, Shen Y, Jin K, Wen Z, Oct;50(10):2790-2798. doi: 10.1161/STROKEAHA.119.026259. ell Metab. 2019 Cao W, Wu B, Wen R, Tian L, Berry GJ, Goronzy JJ, Weyand CM. C Human genome-edited hematopoietic stem cells phenotypically correct Sep 3;30(3):477-492.e6. doi: 10.1016/j.cmet.2019.06.016. Mucopolysaccharidosis type I. Gomez-Ospina N, Scharenberg SG, Mostrel N, In Vivo Translation of the CIRPI System: Revealing Molecular Pathology of Bak RO, Mantri S, Quadros RM, Gurumurthy CB, Lee C, Bao G, Suarez CJ, Khan Rabbit Aortic Atherosclerotic Plaques. Zaman RT, Yousefi S, Chibana H, Ikeno F, S, Sawamoto K, Tomatsu S, Raj N, Attardi LD, Aurelian L, Porteus MH. Nat Long SR, Gambhir SS, Chin FT, McConnell MV, Xing L, Yeung A. J Nucl Med. 2019 Commun. 2019 Sep 6;10(1):4045. doi: 10.1038/s41467-019-11962-8. Sep;60(9):1308-1316. doi: 10.2967/jnumed.118.222471. Components of genetic associations across 2,138 phenotypes in the UK Mechanisms underlying T cell ageing. Goronzy JJ, Weyand CM. Nat Rev Biobank highlight adipocyte biology. Tanigawa Y, Li J, Justesen JM, Horn H, Immunol. 2019 Sep;19(9):573-583. doi: 10.1038/s41577-019-0180-1. Aguirre M, DeBoever C, Chang C, Narasimhan B, Lage K, Hastie T, Park CY, Bejerano G, Ingelsson E, Rivas MA. Nat Commun. 2019 Sep 6;10(1):4064. doi: Detailed Functional Characterization of a Waist-Hip Ratio Locus in 7p15.2 10.1038/s41467-019-11953-9. Defines an Enhancer Controlling Adipocyte Differentiation.Castillejo-Lopez C, Pjanic M, Pirona AC, Hetty S, Wabitsch M, Wadelius C, Quertermous T, Arner E, Prognostic Value of Coronary Microvascular Function Measured Immediately Ingelsson E. iScience. 2019 Sep 10;20:42-59. doi: 10.1016/j.isci.2019.09.006. After Percutaneous Coronary Intervention in Stable Coronary Artery Disease: An International Multicenter Study. Nishi T, Murai T, Ciccarelli G, Shah SV, Early invasive assessment of the coronary microcirculation predicts Kobayashi Y, Derimay F, Waseda K, Moonen A, Hoshino M, Hirohata A, Yong ASC, subsequent acute rejection after heart transplantation.Okada K, Honda Y, Ng MKC, Amano T, Barbato E, Kakuta T, Fearon WF. Circ Cardiovasc Interv. 2019 Luikart H, Yock PG, Fitzgerald PJ, Yeung AC, Valantine HA, Khush KK, Fearon WF. Sep;12(9):e007889. doi: 10.1161/CIRCINTERVENTIONS.119.007889. Int J Cardiol. 2019 Sep 1;290:27-32. doi: 10.1016/j.ijcard.2019.04.018. Cardioaortic replacement for a ruptured root pseudoaneurysm with pulsatile Dynamic CT myocardial perfusion imaging. Nieman K, Balla S. J Cardiovasc subcutaneous extension. Wang H, Shudo Y, Hittinger SA, Woo YJ. Eur J Comput Tomogr. 2019 Sep 11. pii: S1934-5925(19)30279-5. doi: 10.1016/j. Cardiothorac Surg. 2019 Sep 1;56(3):615-617. doi: 10.1093/ejcts/ezy447. jcct.2019.09.003. Heart-lung transplantation with concomitant aortic arch reconstruction for Time-to-operation does not predict outcome in acute type A aortic dissection Eisenmenger syndrome and type B interrupted aortic arch. Wang H, Shudo complicated by neurologic injury at presentation. Chiu P, Rotto TJ, Goldstone Y, MacArthur JW, Woo YJ. J Heart Lung Transplant. 2019 Sep 11. pii: S1053- AB, Whisenant JB, Woo YJ, Fischbein MP. J Thorac Cardiovasc Surg. 2019 2498(19)31669-9. doi: 10.1016/j.healun.2019.09.002. Sep;158(3):665-672. doi: 10.1016/j.jtcvs.2018.12.023. Successful orthotopic heart transplantation in a patient with Marfan syndrome. Harmonizing Genetic Ancestry and Self-identified Race/Ethnicity in Genome- Ogawa Y, Choi CW, Shudo Y, Woo YJ. J Card Surg. 2019 Sep;34(9):875-876. doi: wide Association Studies. Fang H, Hui Q, Lynch J, Honerlaw J, Assimes TL, 10.1111/jocs.14129. Huang J, Vujkovic M, Damrauer SM, Pyarajan S, Gaziano JM, DuVall SL, O'Donnell CJ, Cho K, Chang KM, Wilson PWF, Tsao PS; VA Million Veteran Improving the engraftment and integration of cell transplantation for cardiac Program, Sun YV, Tang H. Am J Hum Genet. 2019 Oct 3;105(4):763-772. doi: regeneration. Tu C, Mezynski R, Wu JC. Cardiovasc Res. 2019 Sep 3. pii: cvz237. 10.1016/j.ajhg.2019.08.012. doi: 10.1093/cvr/cvz237. Pharmacological antagonism of histamine H2R ameliorated L-DOPA-induced Vismione B Interferes with Trypanosoma cruzi Infection of Vero Cells and dyskinesia via normalization of GRK3 and by suppressing FosB and ERK in Human Stem Cell-Derived Cardiomyocytes. Sass G, Tsamo AT, Chounda GAM, PD. Ahmed MR, Jayakumar M, Ahmed MS, Zamaleeva AI, Tao J, Li EH, Job JK, Nangmo PK, Sayed N, Bozzi A, Wu JC, Nkengfack AE, Stevens DA. Am J Trop Med Pittenger C, Ohtsu H, Rajadas J. Neurobiol Aging. 2019 Sep;81:177-189. doi: Hyg. 2019 Sep 30. doi: 10.4269/ajtmh.19-0350. 10.1016/j.neurobiolaging.2019.06.004.

cvi.stanford.edu | 15 Automated Quantification of Diseased Thoracic Aortic Longitudinal Centerline OCTOBER and Surface Curvatures. Bondesson JH, Suh GY, Lundh T, Lee JT, Dake MD, Cheng C. J Biomech Eng. 2019 Oct 1. doi: 10.1115/1.4045271. PMID: 31633168 Multidisciplinary approach utilizing early, intensive physical rehabilitation to accelerate recovery from veno-venous extracorporeal membrane oxygenation. Methamphetamine use association with pulmonary diseases: a retrospective Zhu Y, Bankar D, Shudo Y, Woo YJ. Eur J Cardiothorac Surg. 2019 Oct 1;56(4):811- investigation of hospital discharges in California from 2005 to 2011. Tsai H, Lee 812. doi: 10.1093/ejcts/ezz042. PMID: 30796438 J, Hedlin H, Zamanian RT, de Jesus Perez VA. ERJ Open Res. 2019 Oct 15;5(4). pii: 00017-2019. doi: 10.1183/23120541.00017-2019. PMID: 31637253 Rare Pulmonary Neuroendocrine Cells Are Stem Cells Regulated by Rb, p53, and Notch. Ouadah Y, Rojas ER, Riordan DP, Capostagno S, Kuo CS, Krasnow The impact of prescribed fire versus wildfire on the immune and cardiovascular MA. Cell. 2019 Oct 3;179(2):403-416.e23. doi: 10.1016/j.cell.2019.09.010. PMID: systems of children. Prunicki M, Kelsey R, Lee J, Zhou X, Smith E, Haddad F, Wu 31585080 J, Nadeau K. Allergy. 2019 Oct;74(10):1989-1991. doi: 10.1111/all.13825. PMID: 31002401 De novo mutations in mitochondrial DNA of iPSCs produce immunogenic neoepitopes in mice and humans. Deuse T, Hu X, Agbor-Enoh S, Koch M, Mitral chordae tendineae force profile characterization using a posterior Spitzer MH, Gravina A, Alawi M, Marishta A, Peters B, Kosaloglu-Yalcin Z, Yang ventricular anchoring neochordal repair model for mitral regurgitation in a Y, Rajalingam R, Wang D, Nashan B, Kiefmann R, Reichenspurner H, Valantine three-dimensional-printed ex vivo left heart simulator.Paulsen MJ, Imbrie- H, Weissman IL, Schrepfer S. Nat Biotechnol. 2019 Oct;37(10):1137-1144. doi: Moore AM, Wang H, Bae JH, Hironaka CE, Farry JM, Lucian HJ, Thakore AD, 10.1038/s41587-019-0227-7. PMID: 31427818 MacArthur JW, Cutkosky MR, Woo YJ. Eur J Cardiothorac Surg. 2019 Oct 22. pii: ezz258. doi: 10.1093/ejcts/ezz258. PMID: 31638697 Anatomically specific reactive oxygen species production participates in Marfan syndrome aneurysm formation. Emrich F, Penov K, Arakawa M, Integrating blockchain technology with artificial intelligence for cardiovascular Dhablania N, Burdon G, Pedroza AJ, Koyano TK, Kim YM, Raaz U, Connolly AJ, medicine. Krittanawong C, Rogers AJ, Aydar M, Choi E, Johnson KW, Wang Z, Iosef C, Fischbein MP. J Cell Mol Med. 2019 Oct;23(10):7000-7009. doi: 10.1111/ Narayan SM. Nat Rev Cardiol. 2019 Oct 11. doi: 10.1038/s41569-019-0294-y. PMID: jcmm.14587. PMID: 31402541 31605093 Evaluation of Risk Factors for Heart-Lung Transplant Recipient Outcome: Association between patient age at implant and outcomes after transcatheter An Analysis of the United Network for Organ Sharing Database. Shudo pulmonary valve replacement in the multicenter Melody valve trials. Armstrong Y, Wang H, Lingala B, He H, Kim FY, Hiesinger W, Lee AM, Boyd JH, Currie AK, Berger F, Jones TK, Moore JW, Benson LN, Cheatham JP, Turner DR, Rhodes M, Woo YJ. Circulation. 2019 Oct 8;140(15):1261-1272. doi: 10.1161/ JF, Vincent JA, Zellers T, Lung TH, Eicken A, McElhinney DB. Catheter Cardiovasc CIRCULATIONAHA.119.040682. PMID: 31589491 Interv. 2019 Oct 1;94(4):607-617. doi: 10.1002/ccd.28454. PMID: 31419019 Interfacility Transfer of Medicare Beneficiaries With Acute Type A Aortic Accelerating cardiovascular model building with convolutional neural Dissection and Regionalization of Care in the United States. Goldstone AB, networks. Maher G, Wilson N, Marsden A. Med Biol Eng Comput. 2019 Chiu P, Baiocchi M, Lingala B, Lee J, Rigdon J, Fischbein MP, Woo YJ. Circulation. Oct;57(10):2319-2335. doi: 10.1007/s11517-019-02029-3. PMID: 31446517 2019 Oct 8;140(15):1239-1250. doi: 10.1161/CIRCULATIONAHA.118.038867. PMID: Graph Convolutional Neural Networks for Predicting Drug-Target Interactions. 31589488 Torng W, Altman RB. J Chem Inf Model. 2019 Oct 28;59(10):4131-4149. doi: A Changing Landscape of Mortality for Systemic Light Chain Amyloidosis. 10.1021/acs.jcim.9b00628. PMID: 31580672 Barrett CD, Dobos K, Liedtke M, Tuzovic M, Haddad F, Kobayashi Y, Lafayette R, Stem cells: will they cure pediatric heart failure? Bernstein D. Curr Opin Pediatr. Fowler MB, Arai S, Schrier S, Witteles RM. JACC Heart Fail. 2019 Nov;7(11):958- 2019 Oct;31(5):617-622. doi: 10.1097/MOP.0000000000000801. PMID: 31335749 966. doi: 10.1016/j.jchf.2019.07.007. Comparing Single Cell Versus Pellet Encapsulation of Mesenchymal Stem Cells Heterogeneity in old fibroblasts is linked to variability in reprogramming and in Three-Dimensional Hydrogels for Cartilage Regeneration. Rogan H, Ilagan wound healing. Mahmoudi S, Mancini E, Xu L, Moore A, Jahanbani F, Hebestreit F, Yang F. Tissue Eng Part A. 2019 Oct;25(19-20):1404-1412. doi: 10.1089/ten. K, Srinivasan R, Li X, Devarajan K, Prélot L, Ang CE, Shibuya Y, Benayoun BA, TEA.2018.0289. PMID: 30672386 Chang ALS, Wernig M, Wysocka J, Longaker MT, Snyder MP, Brunet A. Nature. 2019 Oct;574(7779):553-558. doi: 10.1038/s41586-019-1658-5. PMID: 31645721 NOVEMBER Utility of High-Sensitivity and Conventional Troponin in Patients Undergoing Transcatheter Aortic Valve Replacement: Incremental Prognostic Value to Impact of iodine concentration and iodine delivery rate on contrast B-type Natriuretic Peptide. 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cvi.stanford.edu | 17 Leadership

Joseph C. Wu, MD, PhD Director, Stanford Cardiovascular Institute Robert A. Harrington, MD Simon H. Stertzer, MD, Professor of Medicine Arthur L. Bloomfield Professor of Medicine and Radiology Chair, Dept. of Medicine

Ronald L. Dalman, MD Walter C. and Elsa R. Chidester Stephen J. Roth, MD, MPH Professor of Surgery Professor and Chief, Pediatric Cardiology Chief, Division of Vascular Surgery Director, Children’s Heart Center

Michael Snyder, PhD Dominik Fleischmann, MD Professor and Chair, Dept. of Genetics Professor, Dept. of Radiology Director, Stanford Center for Genomics Chief, Cardiovascular Imaging and Personalized Medicine

Kenneth Mahaffey, MD Y. Joseph Woo, MD Professor, Dept. of Medicine Norman E. Shumway Professor Vice Chair of Medicine in Cardiothoracic Surgery for Clinical Research Chair, Dept. of Cardiothoracic Surgery

Mark Nicolls, MD The Stanford Professor of Pulmonary and Alan Yeung, MD Critical Care Medicine, Dept. of Medicine, Li Ka Shing Professor of Medicine Chief, Pulmonary and Critical Co-Chief (Clinical), Care Medicine Division of Cardiovascular Medicine

Paul Yock, MD Martha Meier Weiland Professor, Tom Quertermous, MD Bioengineering and Medicine; William G. Irwin Professor of Medicine and Professor, by courtesy, Co-Chief (Research), of Mechanical Engineering, Division of Cardiovascular Medicine Director, Byers Center for Biodesign

Marlene Rabinovitch, MD Dwight and Vera Dunlevie Professor in Pediatric Cardiology cvi.stanford.edu | 18 © Stanford Cardiovascular Institute 265 Campus Drive West, G1120 Stanford, CA 94305

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