Rapid deployment of SARS-CoV-2 testing: The CLIAHUB

Abstract

About the Authors: Emily D. Crawford Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Department of Microbiology and Immunology, San Francisco, California, United States of America Irene Acosta Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Vida Ahyong Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Erika C. Anderson Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Shaun Arevalo Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Daniel Asarnow Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Shannon Axelrod Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Patrick Ayscue Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Camillia S. Azimi Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Caleigh M. Azumaya Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Stefanie Bachl Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Iris Bachmutsky Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Aparna Bhaduri Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Jeremy Bancroft Brown Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Joshua Batson Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Astrid Behnert Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Ryan M. Boileau Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Saumya R. Bollam Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Alain R. Bonny Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America David Booth Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America Michael Jerico B. Borja Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America David Brown Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Bryan Buie Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Cassandra E. Burnett Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Lauren E. Byrnes Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Katelyn A. Cabral Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, University of California San Francisco, Institute for Neurodegenerative Diseases, San Francisco, California, United States of America Joana P. Cabrera Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Saharai Caldera Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Division of Infectious Disease, San Francisco, California, United States of America Gabriela Canales Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Gloria R. Castañeda Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Agnes Protacio Chan Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Christopher R. Chang Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Arthur Charles-Orszag Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America Carly Cheung Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Unseng Chio Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Eric D. Chow Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America Y. Rose Citron Affiliation: University of California, Berkeley, California, United States of America Allison Cohen Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Lillian B. Cohn Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Department of Experimental Medicine, San Francisco, California, United States of America Charles Chiu Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America Mitchel A. Cole Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Daniel N. Conrad Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Angela Constantino Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Andrew Cote Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Tre’Jon Crayton-Hall Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Spyros Darmanis Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Angela M. Detweiler Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Rebekah L. Dial Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America Shen Dong Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Elias M. Duarte Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America David Dynerman Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Rebecca Egger Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Alison Fanton Affiliation: University of California, Berkeley, California, United States of America Stacey M. Frumm Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Becky Xu Hua Fu Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Valentina E. Garcia Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America Julie Garcia Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Christina Gladkova Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America Miriam Goldman Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Rafael Gomez-Sjoberg Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America M. Grace Gordon Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America James C. R. Grove Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Shweta Gupta Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Alexis Haddjeri-Hopkins Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Pierce Hadley Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, University of California San Francisco, Institute for Neurodegenerative Diseases, San Francisco, California, United States of America John Haliburton Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Samantha L. Hao Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America George Hartoularos Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Nadia Herrera Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Melissa Hilberg Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America Kit Ying E. Ho Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Nicholas Hoppe Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Shayan Hosseinzadeh Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Conor J. Howard Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Jeffrey A. Hussmann Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Elizabeth Hwang Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Danielle Ingebrigtsen Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Julia R. Jackson Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Ziad M. Jowhar Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America Danielle Kain Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America James Y. S. Kim Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Amy Kistler Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America Oriana Kreutzfeld Affiliation: University of California San

About the Authors:

Emily D. Crawford

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Department of Microbiology and Immunology, San Francisco, California, United States of America

Irene Acosta

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Vida Ahyong

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Erika C. Anderson

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Shaun Arevalo

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Daniel Asarnow

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Shannon Axelrod

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Patrick Ayscue

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Camillia S. Azimi

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Caleigh M. Azumaya

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Stefanie Bachl

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Iris Bachmutsky

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Aparna Bhaduri

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jeremy Bancroft Brown

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Joshua Batson

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Astrid Behnert

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Ryan M. Boileau

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Saumya R. Bollam

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Alain R. Bonny

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

David Booth

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Michael Jerico B. Borja

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

David Brown

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Bryan Buie

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Cassandra E. Burnett

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Lauren E. Byrnes

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Katelyn A. Cabral

Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, University of California San Francisco, Institute for Neurodegenerative Diseases, San Francisco, California, United States of America

Joana P. Cabrera

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Saharai Caldera

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Division of Infectious Disease, San Francisco, California, United States of America

Gabriela Canales

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Gloria R. Castañeda

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Agnes Protacio Chan

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Christopher R. Chang

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Arthur Charles-Orszag

Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America

Carly Cheung

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Unseng Chio

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Eric D. Chow

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Y. Rose Citron

Affiliation: University of California, Berkeley, California, United States of America

Allison Cohen

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Lillian B. Cohn

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Department of Experimental Medicine, San Francisco, California, United States of America

Charles Chiu

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Mitchel A. Cole

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Daniel N. Conrad

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Angela Constantino

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Andrew Cote

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Tre’Jon Crayton-Hall

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Spyros Darmanis

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Angela M. Detweiler

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Rebekah L. Dial

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Shen Dong

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Elias M. Duarte

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

David Dynerman

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Rebecca Egger

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Alison Fanton

Affiliation: University of California, Berkeley, California, United States of America

Stacey M. Frumm

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Becky Xu Hua Fu

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Valentina E. Garcia

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Julie Garcia

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Christina Gladkova

Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, Howard Hughes Medical Institute, Chevy Chase, Maryland, United States of America

Miriam Goldman

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Rafael Gomez-Sjoberg

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

M. Grace Gordon

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

James C. R. Grove

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Shweta Gupta

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Alexis Haddjeri-Hopkins

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Pierce Hadley

Affiliations University of California San Francisco, School of Medicine, San Francisco, California, United States of America, University of California San Francisco, Institute for Neurodegenerative Diseases, San Francisco, California, United States of America

John Haliburton

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Samantha L. Hao

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

George Hartoularos

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Nadia Herrera

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Melissa Hilberg

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Kit Ying E. Ho

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Nicholas Hoppe

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Shayan Hosseinzadeh

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Conor J. Howard

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jeffrey A. Hussmann

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Elizabeth Hwang

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Danielle Ingebrigtsen

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Julia R. Jackson

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Ziad M. Jowhar

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Danielle Kain

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

James Y. S. Kim

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Amy Kistler

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Oriana Kreutzfeld

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jessie Kulsuptrakul

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Andrew F. Kung

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Charles Langelier

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Division of Infectious Disease, San Francisco, California, United States of America

Matthew T. Laurie

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Lena Lee

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Kun Leng

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Kristoffer E. Leon

Affiliation: Gladstone Institute, San Francisco, California, United States of America

Manuel D. Leonetti

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Sophia R. Levan

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Sam Li

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Aileen W. Li

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jamin Liu

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Heidi S. Lubin

Affiliation: eSix Development, Oakland, California, United States of America

Amy Lyden

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Jennifer Mann

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Sabrina Mann

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Gorica Margulis

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Diana M. Marquez

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Bryan P. Marsh

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Calla Martyn

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Elizabeth E. McCarthy

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Aaron McGeever

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Alexander F. Merriman

Affiliation: Gladstone Institute, San Francisco, California, United States of America

Lauren K. Meyer

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Steve Miller

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Megan K. Moore

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Cody T. Mowery

Affiliation: Gladstone Institute, San Francisco, California, United States of America

Tanzila Mukhtar

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Lusajo L. Mwakibete

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Noelle Narez

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Norma F. Neff

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Lindsay A. Osso

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Diter Oviedo

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Suping Peng

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Maira Phelps

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Kiet Phong

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Peter Picard

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Lindsey M. Pieper

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Neha Pincha

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Angela Oliveira Pisco

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Angela Pogson

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Sergei Pourmal

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Robert R. Puccinelli

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Andreas S. Puschnik

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Elze Rackaityte

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Preethi Raghavan

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Madhura Raghavan

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

James Reese

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Joseph M. Replogle

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Hanna Retallack

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Helen Reyes

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Donald Rose

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Marci F. Rosenberg

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Estella Sanchez-Guerrero

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Sydney M. Sattler

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Laura Savy

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Stephanie K. See

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Kristin K. Sellers

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Paula Hayakawa Serpa

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Division of Infectious Disease, San Francisco, California, United States of America

Maureen Sheehy

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Jonathan Sheu

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Sukrit Silas

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jessica A. Streithorst

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Jack Strickland

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Doug Stryke

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Sara Sunshine

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Peter Suslow

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Renaldo Sutanto

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Serena Tamura

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Michelle Tan

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Jiongyi Tan

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Alice Tang

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Cristina M. Tato

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Jack C. Taylor

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Iliana Tenvooren

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Erin M. Thompson

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Edward C. Thornborrow

Affiliation: University of California San Francisco, Department of Laboratory Medicine, San Francisco, California, United States of America

Eric Tse

Affiliation: Joint Bioengineering Graduate Program, University of California, Berkeley, California, United States of America

Tony Tung

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Marc L. Turner

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Victoria S. Turner

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Rigney E. Turnham

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Mary J. Turocy

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Trisha V. Vaidyanathan

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Ilia D. Vainchtein

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Manu Vanaerschot

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Sara E. Vazquez

Affiliation: University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

Anica M. Wandler

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Anne Wapniarski

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

James T. Webber

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Zara Y. Weinberg

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Alexandra Westbrook

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Allison W. Wong

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Emily Wong

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Gajus Worthington

Affiliation: Chan Zuckerberg Biohub, San Francisco, California, United States of America

Fang Xie

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Albert Xu

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Terrina Yamamoto

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Ying Yang

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Fauna Yarza

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Yefim Zaltsman

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Tina Zheng

Affiliation: University of California San Francisco, School of Medicine, San Francisco, California, United States of America

Joseph L. DeRisi

* E-mail: [email protected]

Affiliations Chan Zuckerberg Biohub, San Francisco, California, United States of America, University of California San Francisco, Department of Biochemistry and Biophysics, San Francisco, California, United States of America

ORCID logo https://orcid.org/0000-0002-4611-9205

Citation: Crawford ED, Acosta I, Ahyong V, Anderson EC, Arevalo S, Asarnow D, et al. (2020) Rapid deployment of SARS-CoV-2 testing: The CLIAHUB. PLoS Pathog 16(10): e1008966. https://doi.org/10.1371/journal.ppat.1008966

Editor: Carolyn B. Coyne, University of Pittsburgh, UNITED STATES

Published: October 28, 2020

Copyright: © 2020 Crawford et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

Funding: This work was funded by the Chan Zuckerberg Biohub and the Chan Zuckerberg Initiative.

Competing interests: The authors have declared that no competing interests exist.

Accurate diagnostic testing is at the center of controlling infectious disease outbreaks. It allows clinicians and public health practitioners to identify and treat infected individuals as well as inform larger public health interventions (such as quarantine) to prevent new infections. The emergence of the Severe Acute Respiratory Syndrome Coronavirus 2 (SARS-CoV-2)/Coronavirus Disease 2019 (COVID-19) pandemic in the human population in November 2019 has spotlighted the importance of diagnostic testing as a (foundational) bedrock to understand how infections occur and spread. Remarkably, multiple studies now show that asymptomatic and presymptomatic individuals are drivers of community transmission [1]. Thus, broad testing capability is necessary to quell resurgence of outbreaks and reopen the global economy.

Laboratory barriers to testing include the limited availability of space, high-capital infrastructure (robotics and information systems), material resources with uninterrupted supply chains, and trained personnel qualified to conduct assays in Clinical Laboratory Improvement Amendment (CLIA)-approved laboratories. However, sizable untapped capacity exists throughout the United States in a multitude of university research laboratories. Theoretically, this capacity could be directed to rapidly expand emergency response capabilities; however, real barriers exist to their entry into clinical diagnostic testing. Research laboratories—while working with the same suite of methods and from the same biological principles as clinical diagnostic laboratories—have substantively different workflows, expectations of quality control and validation, information management, documentation, traceability, reporting, and regulatory compliance. For research scientists, this burden may appear extremely formidable.

To address the dearth of testing availability in the San Francisco Bay Area, the Chan Zuckerberg Biohub, in partnership with the University of California, San Francisco (UCSF) Clinical Microbiology Lab, rapidly built and deployed an emergency COVID-19 viral testing facility, staffed by a combination of Biohub employees and UCSF graduate students, postdocs, and faculty. These efforts were facilitated by guidance from the Food and Drug Administration (FDA) on February 29, 2020, “Policy for Coronavirus Disease-2019 Tests During the Public Health Emergency” [2], and an Executive Order (March 12, 2020) from California State Governor Gavin Newsom modifying certain California-specific regulatory personnel requirements [3]. The goal of this facility, called the “CLIAHUB,” was to provide free, rapid, high-capacity testing services to local hospitals, Department of Public Health offices, and community-based clinical screening efforts in the San Francisco Bay Area, with a particular emphasis on underserved populations. In this perspective piece, and in the accompanying document [4], we describe in detail the experiences of the Biohub, including our organizational structure, recruitment and training of highly skilled volunteers, automation, information management, engineering, protocol development, and clinical validation. We share the lessons we learned and offer guidance to other research laboratories pursuing rapid expansion of diagnostic capabilities in the context of emergency response for COVID-19 and future pandemic responses.

The Chan Zuckerberg Biohub is a nonprofit research institute that employs approximately 110 people organized into multiple smaller research groups, with nearly half of the staff focused on infectious disease research. The organization’s strong focus on collaborative work, communication, and open science allowed frictionless redistribution of personnel priorities into COVID-19 work. On March 12, 2020, the Biohub’s COVID-19 response staff was organized into 13 work teams (staff members from various research groups and seniority levels were appointed as Team Leads and Backup Team Leads according to their skills and experience). To ensure continuity in the event of an outbreak, laboratory infection control procedures were developed, and all job functions and critical knowledge were held by at least 2 individuals. Communications were facilitated by daily all-hands meetings and dedicated Slack channels. Once clinical testing was underway, volunteers from UCSF were trained to run the assay and organized into 4 nonoverlapping squads to reduce viral transmission risk.

Clinical laboratories are required to meet all applicable federal, state, and local regulations in order to perform patient testing and have to be certified with their state and the Center for Medicare and Medicaid Services (CMS) under CLIA. These regulations specify the laboratory organizational structure and minimum operational standards, with major areas covering the laboratory environment, staffing roles and requirements, information tracking and management, testing validation and procedures, quality assurance, and proficiency testing. Each of these areas had to be addressed with compliance documentation as the CLIAHUB was formed. Ensuring regulatory compliance required close collaboration between the CLIA laboratory director, microbiology section director, and clinical quality assurance and Biohub laboratory lead staff. Since the CLIA laboratory director is ultimately responsible for the operations and quality of test results reported by the laboratory, the importance of this close partnership between the UCSF clinical laboratory and the Biohub cannot be overstated.

The complete CLIAHUB workflow is detailed in Fig 1B and the linked document. Briefly, the CLIAHUB workflow begins with medical courier or shipping company delivered patient samples (nasopharyngeal (NP) or oropharyngeal (OP) swabs). In order to preserve RNA integrity and maximize sensitivity, DNA/RNA Shield was chosen for the transport media. After receipt, patient information was recorded (“accessioned”), and tubes were barcoded, de-swabbed, and queued for transfer into 96 well plates. Transfer from tubes to plates was achieved using both do-it-yourself (“DYI”) engineered and commercial automated solutions. Eight stations using high-speed liquid handlers were used to extract viral RNA, after which reverse transcription polymerase chain reaction (RT-PCR) was run using probes for both the N and E gene of SARS-CoV-2. All reagents and samples were tracked using a custom serverless laboratory information system (LIS). After assay optimization, limit of detection (LOD) was established by serial dilution of a quantified high-titer patient sample, and validation of the assay for the Emergency Use Authorization (EUA) application was achieved by retesting samples previously identified as positive or negative based on a previously approved assay at the UCSF clinical lab.

[Figure omitted. See PDF.]

Fig 1.

(A) Counties served by CLIAHUB and the growth of testing volume over the first 120 days of operation. The most frequent users of testing at CLIAHUB were the surrounding Bay Area counties; however, outlying areas, such as Placer and Lassen, were also frequent users despite the distance. (B) CLIAHUB testing workflow and approximate timing are shown on normalized to a single sample, for preanalytical (blue), analytical (red), and postanalytical (green/yellow). The time to process a batch of 84 samples was approximately 6.7 h, including preanalytical and postanalytical steps. Median TAT was 24 h, highlighting the variability in extrinsic factors not under laboratory control, such as medical courier delivery times. qPCR, quantitative polymerase chain reaction; TAT, turnaround time.

https://doi.org/10.1371/journal.ppat.1008966.g001

On March 20, 2020, 8 days after starting this project, the CLIAHUB returned its first clinical result. As of this writing (October 17, 2020), the CLIAHUB has returned 151,795 clinical results. A total of 36 California county Department of Public Health (“DPH”), safety net hospitals, jails, skilled nursing facilities, and public clinics have utilized the CLIAHUB for SARS-CoV-2 testing (Fig 1), in addition to community-based studies. In the period from May 8 to June 8, 2020, the CLIAHUB processed over 1,300 samples on average per day. The maximum number of samples processed in a single day was 2,688. Median turnaround time (TAT) was 24 h. For genomic epidemiology, positive samples were routed for full SARS-CoV-2 genome sequencing [1]. While the samples processed by CLIAHUB were heterogeneous and not representative of the general population, several important characteristics of the disease and the test were notable. A broad range of cycle threshold (Ct) values have been observed (from 7 to 45), indicative of a tremendous range of viral loads within this disease. Samples were considered positive if the Ct for both the N and E gene probes were less than 40 for the original standard operating procedure (SOP). If a sample was positive for 1 of the 2 probes, the result was considered indeterminant. In subsequent iterations of the protocol, samples were considered positive if either of the 2 probes were below a Ct of 40. While there was an excellent agreement between both viral probes, in 9% of cases, only 1 of the 2 probes were detected, suggesting that assays that rely on detection of a single gene alone may have a significant false negative rate (Fig 2).

[Figure omitted. See PDF.]

Fig 2. Concordance between RT-PCR Ct values for the E and N gene probes.

For 91% of samples, agreement between viral gene probe sets were within 5 Ct cycles, with the majority within 2 cycles. For 9% of samples, only 1 gene was detected (5% E gene only, 4% N gene only), leading to an indeterminate result. In all such cases, the sample extraction and RT-PCR was repeated; points plotted represent the retest result. Ct, cycle threshold; ND not detected; RT-PCR, reverse transcription polymerase chain reaction.

https://doi.org/10.1371/journal.ppat.1008966.g002

The largest users of CLIAHUB testing capacity have been Bay Area and outlying county DPHs, including San Mateo, Marin, Alameda, Placer, Tehama, Santa Clara, and Sonoma counties. Feedback from individual counties indicated that access to free and fast testing allowed insight into at-risk populations, which, in turn, led to deployment of medical personnel. In the case of congregate care facilities, intervention and stabilization avoided evacuation of residents to local hospitals. The CLIAHUB also directly enabled community-based studies in the town of Bolinas, the Mission District, and Bayview Hunters Point neighborhoods of San Francisco, and a study of unsheltered persons [1]. These studies provided both clinically actionable results for individuals and communities, in addition to valuable insight about the socioeconomics and demographics of populations that were disproportionately affected. Altogether, the experience of CLIAHUB demonstrates that research facilities can indeed be converted to clinical testing laboratories during a pandemic emergency declaration that are capable of returning high-quality and timely clinical results in order to meet the challenge of a growing pandemic. We hope that the accompanying “How to” document, protocols, and engineering details (dx.doi.org/10.17504/protocols.io.bfi2jkge) will serve as a guide for others in the midst of this or any other future pandemic.

Citation: Crawford ED, Acosta I, Ahyong V, Anderson EC, Arevalo S, Asarnow D, et al. (2020) Rapid deployment of SARS-CoV-2 testing: The CLIAHUB. PLoS Pathog 16(10): e1008966. https://doi.org/10.1371/journal.ppat.1008966

References

1. Chamie G, Marquez C, Crawford E, Peng J, Petersen M, Schwab D, et al. SARS-CoV-2 Community Transmission disproportionately affects Latinx population during Shelter-in-Place in San Francisco. Clin Infect Dis. 2020. pmid:32821935

2. Coronavirus (COVID-19) Update: FDA Issues New Policy to Help Expedite Availability of Diagnostics. U.S. Food & Drug Administration; 2020. https://www.fda.gov/news-events/press-announcements/coronavirus-covid-19-update-fda-issues-new-policy-help-expedite-availability-diagnostics

3. State of California ED. Executive Order N-25-20. https://www.gov.ca.gov/wp-content/uploads/2020/03/3.12.20-EO-N-25-20-COVID-19.pdf

4. Lyden A, Crawford E, Ahyong V, Vanaerschot M, Hayakawa Serpa P, Raghavan P, et al. CLIAHUB Automated RNA Extraction & RT-PCR Protocol V2. https://www.protocols.io/view/cliahub-automated-rna-extraction-amp-rt-pcr-protoc-bfi2jkge/abstract