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Characterizing Long COVID in Children and Adolescents

Authors
Rachel Gross,Tanayott Thaweethai
Lawrence Kleinman,Jessica Snowden,Erika Rosenzweig,Joshua Milner,Kelan Tantisira,Kyung Rhee,Terry Jernigan,Patricia Kinser,Amy Salisbury,David Warburton,Sindhu Mohandas,John Wood,Jane Newburger,Dongngan Truong,Valerie Flaherman,Torri Metz,Elizabeth Karlson,Lori Chibnik,Deepti Pant,Aparna Krishnamoorthy,Richard Gallagher,Michelle Lamendola-Essel,Denise Hasson,Stuart Katz,H. Yin,Benard Dreyer,Megan Carmilani,Karen Coombs,Megan Fitzgerald,Nick Güthe,Mady Hornig,R. Letts,Aimee Peddie,Brittany Taylor,Andrea Foulkes,Melissa Stockwell,Venkataraman Balaraman,Amanda Bogie,Hülya Bükülmez,Allen Dozor,Daniel Eckrich,Amy Elliott,Danielle Evans,Jonathan Farkas,E. Faustino,Laura Vega,Sunanda Gaur,Ashraf Harahsheh,Uzma Hasan,Daniel Hsia,Gredia Huerta-Montañez,Kathy Hummel,Matt Kadish,David Kaelber,Sankaran Krishnan,Jessica Kosut,Jerry Larrabee,Peter Lim,Ian Michelow,Carlos Oliveira,Hengameh Raissy,Zaira Rosario-Pabón,Judith Ross,Alice Sato,Michelle Stevenson,Maria Talavera‐Barber,Ronald Teufel,Kathryn Weakley,Emily Zimmerman,Marie‐Abèle Bind,James Chan,Zoe Guan,Richard Morse,Harrison Reeder,Natacha Akshoomoff,Judy Aschner,Rakesh Bhattacharjee,Lesley Cottrell,Kelly Cowan,Viren D’Sa,Alexander Fiks,Maria Gennaro,Katherine Irby,Manaswitha Khare,Jeremy Guttierrez,Russell McCulloh,Shalu Narang,Manette Cochinwala,Sheila Nolan,Paul Palumbo,Julie Ryu,Juan Salazar,Rangaraj Selvarangan,Cheryl Stein,Alan Werzberger,William Zempsky,Robin Aupperle,Fiona Baker,Marie Banich,Deanna Barch,Arielle Baskin–Sommers,James Bjork,Susan Bookheimer,Sandra Brown,B.J. Casey,Linda Santiago,Duncan Clark,Anders Dale,Mirella Dapretto,Thomas Ernst,Damien Fair,Sarah Ewing,John Foxe,Edward Freedman,Naomi Friedman,Hugh Garavan,Dylan Gee,Raúl González,Kevin Gray,Mary Heitzeg,Megan Herting,Joanna Jacobus,Angela Laird,Christine Larson,Krista Lisdahl,Mónica Luciana,Beatriz Luna,Magdalena Żołędziewska,Erin McGlade,Eva Müller‐Oehring,Bonnie Nagel,Michael Neale,Martin Paulus,Alexandra Potter,Deborah Yurgelun‐Todd,Elizabeth Sowell,Lindsay Squeglia,Susan Tapert,Lucina Uddin,Sylia Wilson,Paul Darden,Lexie Dixon,Amal Ahmed,Claus Garbe,Laura Hobart‐Porter,Almary Akerlundh,Howard Lee,Hannah Krehbiel,Haley Spradlin,P Yount,Akram Alshawabkeh,C McDevitt,Brett Anderson,Chijoke Ikomi,Claudio Katz,Danielle Katz,Karen Kowal,Marisa Meyer,Andrew Atz,Cuong Nguyen,Gwen Pellicciotti,Thao-Ly Phan,Karen Ravin,Victoria Reynolds,Annette Baker,Abigail Strang,Deepika Thacker,Annabelle Goetter,Dithi Banerjee,J. Cheung,Travis Hong,Shanelle Kalua,Elina Minami,Andrea Siu,Micah Tong,Baylea Albarado,Tracey Allen,Allison Attuso,Tracy Ayers,Emily Bebler,Gianfranco Bella,Antonette Bennett,James Brown,Ryan Brown,Alexis Brown,Angela Carville,Sarah Darby,Kara Devall,Amber Dragg,Angela Elderedge,Elisabeth Fontenot,Greta Fry,B. Gildersleeve,Sara Goff,Lauren Harrington,Jackie Boyd,Lisa Jones,V. Kaiser,C. Kaiser,Y.S. Lee,Stephen Lee,Dong Lee,E Lejeune,Robert Leonhard,Jennifer Levatino,Natalie Buchbinder,D. Lewis,Adam Lloyd,Ron Monce,Sophie Munro,M. Phillips,Blair Pucheu,Emily Rachal,Jennifer Rood,Sandrine Roussel,R.D.E. Rumsey,Cynthia Sanford,Virginia Casey,Mônica Santos,Melissa Santos,A. Stafford,Norma Castro,A. Thomassie,C. Waguespack,Katherine Walgamotte,Meredith Welch,Alan Windham,Lindsey Stevenson,Tiffany Bell,L. Bell,Soham Dasgupta,Sarah Deans,Katie Harris,Donna Harris,Laura Harris,Molly Hemmerle,Sarah King,C McGuire,Maryanne Chrisant,B. Merten,Sarah Morris,M. Ray,Birgit Reinhardt,K. Clark,Shellese Shemwell,Theresa Simeon,Katherine Walker,Katharine Clouser,Sara Watson,Tom Connors,Johnathon Figliomeni,John Costello,L Gamboa,Megan Morse,Aleisha Nabower,Evan Roberts,Kari Simonsen,Cathal Cummins,Jessica Bon,Denise Hoover,S Dabney,Marie-Christine Fahrner,Torrey Gallagher,Katharina Martini,Mary McNally,Sarah Stiverson,David Archuleta,Rebecca Brito,Richard Campbell,Jenifer Chávez,Summer Chavez,Walter Dehority,Noelle Garcia-Soberanez,Eve Gronert,Matthew Kadish,Debbie Lovato,Kunxin Luo,Nuria Martı́nez-Navarrete,Analyse Merlino,Maricela Diaz,MaryAnne Sterling,Sarah Ward,Emily Ward,Audrey Dionne,Kevin Wilson,Gina Fergeson,Brittany Karfonta,Ryan McKee,Tiffany Moore,V. Owens,Sarah Stubbs,Timothy VanWagoner,Matthew Elias,Timothy Walsh,Gipsis Román,Inmaculada Ortíz,José Cordero,Josiane Jesus,Cristina Galán,NELMARI OTERO,Maria Robles,Vinicius Faustino,Priscilla Roman,Alex Fiks,Xiodenis Santiago,Carmen Vélez-Vega,Carlos Vergara,Marina Dantas,Tyler Kasmarcak,Daniel Forsha,Kreighton Milks,G. Adam,Rebecca Andrew,Jyoti Angal,M.A. Barber,Shelby Cerkovnik,Carla Reis,Christa Friedrich,Carolina García,S. García,Sonia García,Kellie Geigle,Richard Gyasi,Christine Hockett,Rachel Johannsen,Edward Johnson,Madison Johnson,P. Johnson,Jennifer Lang,Sean Lang,Ezekiel Emanuel,Lorie Miler,Jessica Seiler,Bret Sundleaf,Nic Torbert,Billy Trosper,Jaime Werpy,San‐Lin Young,Laurie Chassereau,Thomas Lahiri,Katherine Rampone,L Lake,Karen Moffett,E Polák,Sarah Stutler,Charlotte Workman,Karen Hasbani,Rosalba Cain,Emma Carpenter,Silvia Rodríguez,Andrew Heath,Neda Moghadam,Candice Mulder,Sharon O’Neil,A Ríos,Sydney Rosen,Natayla Seals,Christina Hester,Andrea Smith,Paulette Smith,Deeba Tabibi,Anthony Hill,T. AQUINO,Elizabeth Berg,Steve Caddle,Marina Catallozzi,William Dobyns,Sophia Chung,Aliva De,Alejandro Pérez,Michael DiLorenzo,Dani Dumitriu,Kanwal Farooqi,Michael Fremed,Sylvie Goldman,Kayla Kaplan,Usha Krishnan,Anita Krishnan,Aimee Layton,Angela Lignelli-Dipple,Son McClaren,Jonathan Overdevest,Michelle Rodriguez,Jay Selman,Wendy Silver,R. Silvério,Ana Romero,Celibell Vargas,Carmen Vargas,D. Caputo,Camille Leggieri,Pamela Pretsch,L. Cerracchio,Amber Folnagy,Sherri Gzemski,Yue Hao,Simon Li,Sandee Moroso,Akhil Patel,Benjamin Richlin,Harsh Sharma,Dany Soto,EungJoon Kim,Do Kim,Christian Suarez,M. Suárez,Bibiana Forero,Emma Bean,Matthew Kluko,Carlie Defelice,Hassan Chebib,Katherine Herbst,Stephanie Lesmes,Norman Schulman,Wilson Pace,Alicia Brooks-Greien,Kovacs Colin,Ariadna Juarez-Colunga,Brian Manning,Joel Shields,Jack Westfall,Daphne York,Lynn Olson,Kristin Davis,Miranda Griffith,Everly Macario,Jennifer Steffes,Alessandra Torres,John Griswold,A Nowakowski,Maeveen Riordan,Rozina Aamir,Mohammed Abuzahrieh,Iris Liu,W. Dalton,Sara Fortuna,Judi Minium,Bonnie Rosolowski,Suzanne Braniecki,Elizabeth Mack,M Contreras,Jennifer Co‐Vu,Suzanne Kaseta,Zachary Messer,Armando Varela‐Ramírez,Aalok Singh,Gautam Singh,Richard Williams,Elizabeth Ricciardi,Vanessa Trespalacios,Yvonne Carter,Brian McCrindle,Kelsye Howell,Megan Mains,Thamyris Regis,Megan Warner,Jeremy Gutierrez,Elizabeth Mitchell,Ileana Matta,César Cabezas,Cinthia Sanchez,Maria Arroyo,Baohua Chao,Margarita Holguin,S. Reyes,Wendy Barrientos,Guadalupe Melis,Tony Herrera,Elizabeth Kiernan,Andrea Schreck,Janelle Celso,Laura Franco,Shawn O’Connor,M. Glenn-Arroyo,Juan Gutiérrez,Matt Oster,M. Joskowitz,Christine Moran,David Pyatt,Lisa Vallej,Argelinda Baroni,Thomas Ovalle,J. Fárkas,Maria Isidoro-Chino,Deniz Kesebir,Ashley Quarless,Salman Siddiqui,Ranjini Srinivasan,Moriah Thomason,Phoebe Burton,Rosa Cano-Lorente,Stephanie Wehbe,J Espinoza,Abigail Espinoza,Sara Moyer,Amy Rider,Sally Russell,Mark Russell,M.G. Schecter,Suchitra Rao,José Aguilar,David Benjamin,Brian Emerson,Jennifer Graves,Amanda Guerrero,Janosch Linkersdoerfer,Robert Schooley,Wes Thompson,Thanh Trinh,Ron Yang,C. Cisneros,Lauren Goedde,Cedric Manlhiot,Jorge Limia,Melanie Curry,Nour El-Sabbagh,Samuel Agbeh,Christopher Herring,Yamuna Sanil,B. McKenzie,Aparicio Morales,Ian Colrain,Ingrid Durley,Carlos Caldera,Jennifer Dzul,Claudia Zárate,Paola Badilla,Jennifer Keith,Kumar Gaurav,Daniel Messinger,Katie Prazak,Sara Nixon,Melanie Cardoso,Meagan Sullivan,Nancy Sullivan,Sylvie Villard,Christine Cloak,Huajun Liang,Greg Ryan,Mary Heitzerg,J. CONLEY,Leon Puttler,Shubhika Srivastava,William Iacono,Alan Schroeder,Megan Retucci,Sile Mhurchu,Samantha Spallina,Kirsten Cline,Lauren Heinrich,Perry Renshaw,Jackie Szmuszkovicz,Christopher Barrett,Sofia Lozon,Scott Spear,Tory Clearwater,Christine Kaiver,Christopher Nelson,Zach Paltzer,Bridgette Peteet,Olive Calonge,Noah Slattery,Lisa Straub,Pamela Madden,Taylor Powell,Denise Schmitz,Boris Epie,Rebekah Hobbs,Alex Williams,Zhiguang Xiang,Julie Miller,Felicia Trachtenberg,Ayesha Amarnath,James Ambrosoli,David Artis,Suresh Bandari,Emily Birmingham,Li Wang,Lozan Eyob,Kerri Hayes,Chenwei Hu,Dara Watkins,Melissa Joyce,E. Joyce,Valentina Kazlova,Amanda Marshall,Devine Mbizdenyuy,Pei‐Fan Mu,Robin Rowe,Brooke Sayles,Mo Zhang,Melissa Burnett,Kolby Sanders-Lewis,Kimberly McHugh,Megan Bickford,Pierre Wong,Jason Buckley,David Dennis,Elizabeth Emrath-Zwick,Mary Freeman,Lanier Jackson,Scott Pletzer,Natasha Ruth,Carolyn Taylor,Sinai Zyblewski,Andrea Dunn,Lilly Fagatele,Linda Lambert,Kristin Sexson,Elias Moussi,David Olukayode,Sandra Peña,Ricardo Pignatelli,Faridis Serrano,Sara Tejtel,Lara Shekerdemian,Sarah DeFerrantini,Thomas Giorgio,Numaira Khan,Simran Mahanta,Mary Son,Georgia Reis,Fariborz Behzadian,Carlos Cañas,Andrew Cheng,B Scott,Mike Gawad,Alicia Kazarians,Ashot Sarkissian,Consuelo Secules,Jennifer Su,Jodie Votava‐Smith,Sharon Wagner‐Lees,Sanjeev Aggarwal,Aiman Almasnaah,Nirupama Kannikeswaran,Kathleen Meert,Priya Spencer,Sureja Sundaralingam,Vishnu Undyala,Amanda Weber,C Farr,Tamara Bradford,Marla Johnston,C.R. Forrest,Dana Albizem,Susan Coffin,Therese Giglia,Katherine Lupton,Grace Marks,Tonia Morrison,Jennifer Nelson,Rajeev Sachdeva,J. Britton,Alix Fetch,Marisa Almaguer,James Cnota,Lauryn Dugan,E Pickering,Kathleen Rathge,Christine Capone,Nilanjana Misra,Olga Shamailova,Tammy Doman,Sagar Jani,Jessica Bainton,Doris Alaby,Norma Barton,Carol Prospero,Edward Williams,Varsha Zadokar,Arash Sabati,Kylie Domian,Ashley Herzberg,Sudhansoo Khanna,Todd Nowlen,Susan Park,Jade Porche,Samantha Stack,Kirsten Dummer,Sherrie Bandy,Jane Burns,Katheryn Crane,Sanjeet Hedge,Joan Pancheri,Adriana Yock‐Corrales,R. Payne,Mary Stumpf,Michael Portman,Hidemi Kajimoto,Onyekachukwu Osakwe,Jemylle Morato,Divya Shakti,Katrina Golub,Chanel Rojas,Korsin Rosalind,Chantal Sanchez,Kavita Sharma,William Anguiano,Catherine Ikemba,Alejandra Lozano,María Martínez,Wendy Rojas,Stephanie Handler,Joe Block,Regina Cole,Jennifer Maldonado,Pei‐Ni Jone,Michael Carr,Lauren Goodell,Wantanabe Kar,Kathleen Hof,Camden Hebson,Kristal Hock,Lerraughn Morgan,Isaura Macias,Carl Owada,Mayra Rangel,Michelle Sykes,Lisa Newman,J Abella,Quinn Barnette,Christine Bevc,Jennifer Beverly,Julie Croxford,Tonya Farris,Sean Hanlon,David Hines,Vicki Johnson-Lawrence,Craig Lefebvre,Beth Linas,Bryan Luukinen,Manoranjan Mandal,Nikki McKoy,Demian Pasquarelli,Claire Quiner,Rita Sembajwe,Vanessa Thornburg,Kendall Tosco,Hannah Wright,Judith Hochman,Leora Horwitz,Andrea Troxel,Lenard Adler,Precious Akinbo,Ramona Almenana,Malate Aschalew,Lee Balick,Ola Bello,Sultana Bhuiyan,Wei Wang,Ryan Branski,Joshua Briscoe,Shari Brosnahan,Elliott Bueler,Ylanna Burgos,Nina Caplin,David Chaplin,Chen Yu,Cheng Shen,Pyoeng Choe,Joonsup Choi,Alicia Chung,Richard Church,Stanley Cobos,Nicholas Croft,Aaron Irving,Phoebe Boccio,Iván Díaz,Jasmin Divers,Vishal Doshi,Samantha Ebel,Shari Esquenazi-Karonika,Arline Faustin,Elias Febres,Jeffrey Fine,Sandra Fink,Catherine Freeland,Jennifer Frontera,Alejandra González‐Duarte,Sophia Hill,Jobayer Hossain,Md Islam,Christina Jean,Stephen Johnson,Neha Kansal,Rachel Kenney,Tammy Kershner,Deepshikha Kewlani,Jong-Hyeok Kwak,Sarah Laury,Gregory Laynor,Lei Lei,Thomas Leon,Janelle Linton,M Logan,Nadia Malik,Lia Mamistvalova,Hannah Mandel,Gabrielle Maranga,Aprajita Mattoo,Tsarah Mei,Alan Mendelsohn,Emmanuelle Mercier,Patricio Vernetti,Michael Miller,Michael Mitchell,André Moreira,Praveen Mudumbi,Erica Nahin,Nandini Nair,Joseph Nekulak,K Owens,Brendan Parent,Nandan Patibandla,Peter Petrov,Radu Postelnicu,Francesca Pratt,Isabelle Randall,Jagadish Padubidri,Amy Rapkiewicz,John‐Ross Rizzo,Johana Rosas,Chelsea Rose,M. Dönszelmann,Michele Santacatterina,Binita Shah,Aasma Shaukat,Naomi Simon,Aylin Simsir,M Stinson,Wenfei Tang,Vasishta Tatapudi,Sujata Thawani,Mary Thomas,Lorna Thorpe,MeeLee Tom,Ethan Treiha,Jennifer Truong,Mmekom Udosen,Carlos Valencia,José Pérez,Crystal Vidal,Anand Viswanathan,Amy Willerford,Natasha Williams,Crystal Wong,Marion Wood,Shannon Wuller,Chloe Young,Jonah Zaretsky,Susanna Zavlunova,Shawn Murphy,Shreya Ahirwar,Shifa Ahmed,Layne Ainsworth,Rachel Atchley-Challenner,Paul Avilach,Trisha Balan,Nicholas Benik,Barbara Benoit,William Bonaventura,Natalie Boutin,B Brion,Andrew Cagan,Tianrun Cai,Tingyi Cao,Víctor Castro,Xander Cerretani,Simon Chang,David Cheng,Maria Ciriello,Karen Costenbader,Dimitar Dimitrov,Hossein Estiri,Michel Fayad,Candace Feldman,Vivian Gainer,Bhaswati Ghosh,Randy Gollub,Alan Harris,Karl Helmer,A. Hendrix,Ana Holzbach,Weixing Huang,Daniel Kaufman,Diane Keogh,J. Kerr,Jeffrey Klann,Jessica Lasky‐Su,Katherine Liao,Douglas MacFadden,Alberto Malovini,Megan Martel,Michael Mendis,Reeta Metta,Jonathan Monteiro,Eduardo Morales,Marc-Danie Nazaire,Gregory Neils,Amber Nguyen,James Norman,Henry Paik,Heekyong Park,Dustin Rabideau,Kathleen Rossi-Roh,L Santacroce,Katherine Schlepphorst,Carolin Schulte,Caitlin Selvaggi,Daniel Shinnick,William Simons,Lynn Simpson,Michael Flanders,Zachary Strasser,Mitesh Thakrar,Magnus Thörn,Philip Trewett,Dustin Fleet,Kavishwar Wagholikar,Taowei Wang,Nich Wattanasin,Griffin Weber,Mark Williams,Ren Zhang,Mine Cicek,Erik Boysen,Nancy Chang,Thomas Flotte,Erika Frisch,Gary Welch,Samantha Wirkus,Nicole Zahnle,Scott Adams,Teresa Akintonwa,Leyna Aragon,Bryan Bander,Karyn Bishof,Frank Blancero,G. Brooks,Etienne Carignan,Leah Castro-Baucom,Magdalena Cerdá,D Copeland,Claudia Corchado,Hannah Davis,Felicia Blakley,Marissa Diggs,Belinda Edwards,Hannah Brown,Umar Favors,Whitney Fields,Liza Fisher,Alan Gaffney,Margot Witvliet,Roberto García,Tracy Gustafson,Yper Hall,Valerie Holmes,Maxwell Hornig,William Jefferson,Christina Kim,Nancy Kochis,Kevin Kondo,John Lam,Françoise Lawrence,Laura Lerma,J. Lewis,J. Lindsay,Sandra Lopez,Hans‐Peter Marti,Thomas Martínez,Christine Maughan,Lisa McCorkell,Richard McGrath,Travis Minor,Catherine Moore,Khanh Nguyen,Lauren Nichols,Lisa O’Brien,Holly Olson,Alice Perlowski,Elizabeth Lorenzo,Lisa Prentiss,Nadia Raytselis,Lidia Regino,M. Roberts,Nitza Rochez,M. Rockwell,Judith Rutter,Elle Seibert,A. Sekar,Charlotte Smith,Lauren Stiles,Emily Taylor,Julie Thompson,Jason Wiese,Stephen Valdiva,Heather Vincent,Ann Wallace,Robert Wilensky,Melissa Williams,Neely Williams,Karen Dawson,Andrew Wylam,Mike Zissis,Krishnan Sankaran,Manette Ness-Cochinwala,Elina Hyppönen,Arielle Baskin‐Sommers,B. Casey,Beatríz Luna,Daniel Soto,Rosa Lorente,Cole Smith,Savério Bellusci
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,Elizabeth Hensor
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Aug 21, 2024
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Abstract

Importance Most research to understand postacute sequelae of SARS-CoV-2 infection (PASC), or long COVID, has focused on adults, with less known about this complex condition in children. Research is needed to characterize pediatric PASC to enable studies of underlying mechanisms that will guide future treatment. Objective To identify the most common prolonged symptoms experienced by children (aged 6 to 17 years) after SARS-CoV-2 infection, how these symptoms differ by age (school-age [6-11 years] vs adolescents [12-17 years]), how they cluster into distinct phenotypes, and what symptoms in combination could be used as an empirically derived index to assist researchers to study the likely presence of PASC. Design, Setting, and Participants Multicenter longitudinal observational cohort study with participants recruited from more than 60 US health care and community settings between March 2022 and December 2023, including school-age children and adolescents with and without SARS-CoV-2 infection history. Exposure SARS-CoV-2 infection. Main Outcomes and Measures PASC and 89 prolonged symptoms across 9 symptom domains. Results A total of 898 school-age children (751 with previous SARS-CoV-2 infection [referred to as infected ] and 147 without [referred to as uninfected ]; mean age, 8.6 years; 49% female; 11% were Black or African American, 34% were Hispanic, Latino, or Spanish, and 60% were White) and 4469 adolescents (3109 infected and 1360 uninfected; mean age, 14.8 years; 48% female; 13% were Black or African American, 21% were Hispanic, Latino, or Spanish, and 73% were White) were included. Median time between first infection and symptom survey was 506 days for school-age children and 556 days for adolescents. In models adjusted for sex and race and ethnicity, 14 symptoms in both school-age children and adolescents were more common in those with SARS-CoV-2 infection history compared with those without infection history, with 4 additional symptoms in school-age children only and 3 in adolescents only. These symptoms affected almost every organ system. Combinations of symptoms most associated with infection history were identified to form a PASC research index for each age group; these indices correlated with poorer overall health and quality of life. The index emphasizes neurocognitive, pain, and gastrointestinal symptoms in school-age children but change or loss in smell or taste, pain, and fatigue/malaise–related symptoms in adolescents. Clustering analyses identified 4 PASC symptom phenotypes in school-age children and 3 in adolescents. Conclusions and Relevance This study developed research indices for characterizing PASC in children and adolescents. Symptom patterns were similar but distinguishable between the 2 groups, highlighting the importance of characterizing PASC separately for these age ranges.

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