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Citations to this article

Favorable outcomes of COVID-19 in recipients of hematopoietic cell transplantation
Gunjan L. Shah, … , Genovefa Papanicolaou, Miguel-Angel Perales
Gunjan L. Shah, … , Genovefa Papanicolaou, Miguel-Angel Perales
Published September 8, 2020
Citation Information: J Clin Invest. 2020;130(12):6656-6667. https://doi.org/10.1172/JCI141777.
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Clinical Research and Public Health Article has an altmetric score of 46

Favorable outcomes of COVID-19 in recipients of hematopoietic cell transplantation

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Abstract

BACKGROUND Understanding outcomes and immunologic characteristics of cellular therapy recipients with SARS-CoV-2 is critical to performing these potentially life-saving therapies in the COVID-19 era. In this study of recipients of allogeneic (Allo) and autologous (Auto) hematopoietic cell transplant and CD19-directed chimeric antigen receptor T cell (CAR T) therapy at Memorial Sloan Kettering Cancer Center, we aimed to identify clinical variables associated with COVID-19 severity and assess lymphocyte populations.METHODS We retrospectively investigated patients diagnosed between March 15, 2020, and May 7, 2020. In a subset of patients, lymphocyte immunophenotyping, quantitative real-time PCR from nasopharyngeal swabs, and SARS-CoV-2 antibody status were available.RESULTS We identified 77 patients with SARS-CoV-2 who were recipients of cellular therapy (Allo, 35; Auto, 37; CAR T, 5; median time from cellular therapy, 782 days; IQR, 354–1611 days). Overall survival at 30 days was 78%. Clinical variables significantly associated with the composite endpoint of nonrebreather or higher oxygen requirement and death (n events = 25 of 77) included number of comorbidities (HR 5.41, P = 0.004), infiltrates (HR 3.08, P = 0.032), and neutropenia (HR 1.15, P = 0.04). Worsening graft-versus-host disease was not identified among Allo recipients. Immune profiling revealed reductions and rapid recovery in lymphocyte populations across lymphocyte subsets. Antibody responses were seen in a subset of patients.CONCLUSION In this series of Allo, Auto, and CAR T recipients, we report overall favorable clinical outcomes for patients with COVID-19 without active malignancy and provide preliminary insights into the lymphocyte populations that are key for the antiviral response and immune reconstitution.FUNDING NIH grant P01 CA23766 and NIH/National Cancer Institute grant P30 CA008748.

Authors

Gunjan L. Shah, Susan DeWolf, Yeon Joo Lee, Roni Tamari, Parastoo B. Dahi, Jessica A. Lavery, Josel Ruiz, Sean M. Devlin, Christina Cho, Jonathan U. Peled, Ioannis Politikos, Michael Scordo, N. Esther Babady, Tania Jain, Santosha Vardhana, Anthony Daniyan, Craig S. Sauter, Juliet N. Barker, Sergio A. Giralt, Cheryl Goss, Peter Maslak, Tobias M. Hohl, Mini Kamboj, Lakshmi Ramanathan, Marcel R.M. van den Brink, Esperanza Papadopoulos, Genovefa Papanicolaou, Miguel-Angel Perales

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MA Thompson, JP Henderson, PK Shah, SM Rubinstein, MJ Joyner, TK Choueiri, DB Flora, EA Griffiths, AP Gulati, C Hwang, VS Koshkin, EB Papadopoulos, EV Robilotti, CT Su, EM Wulff-Burchfield, Z Xie, PP Yu, S Mishra, JW Senefeld, DP Shah, JL Warner, B Halmos, A Verma, BA Gartrell, S Goel, N Ohri, RA Sica, A Thakkar, KE Stockerl-Goldstein, O Butt, JL Campian, MA Fiala, R Monahan, AY Zhou, P Bohachek, D Mundt, M Streckfuss, E Tadesse, PE Lammers, SG Revankar, OA Panagiotou, PC Egan, D Farmakiotis, H Khan, AJ Olszewski, A Loaiza-Bonilla, SA Prete, AH Angevine, MH Bar, KM Lo, J Stratton, PL Weinstein, PF Caimi, JS Barnholtz-Sloan, JA Garcia, JM Nakayama, S Gupta, NA Pennell, MS Ahluwalia, SJ Dawsey, A Nizam, CA Lemmon, C Hoppenot, A Li, Z Bakouny, G Bouchard, FJ Busser, JM Conners, CR Curran, GD Demetri, A Giordano, K Kelleher, A Nohria, A Schmidt, G Shaw, EM Allen, PV Nuzzo, W Xu, RL Zon, T Zhang, S Halabi, GH Lyman, JJ Graber, P Grivas, AR Khaki, ET Loggers, RC Lynch, ES Nakasone, MT Schweizer, LM Tachiki, S Vinayak, MJ Wagner, A Yeh, NT Gatson, S Goyal, MP Huynh-Le, LJ Rosenstein, JM Clement, A Daher, ME Dailey, R Elias, E Hsu, AG Menendez, J Rathmann, OK Serrano, A Jayaraj, SM Gadgeel, JE Hawley, DL Hershman, MK Accordino, D Bhutani, GK Schwartz, DY Reuben, S Mushtaq, EH Bernicker, J Deeken, D Shafer, MA Lewis, TD Rhodes, DM Gill, CA Low, S Nagle, B Hayes-Lattin, S McWeeney, ER Nemecek, HA Zaren, SJ Smith, G Nagaraj, M Akhtari, E Lau, ME Reeves, S Berg, D Elms, AK Morgans, FH Wehbe, J Altman, M Gurley, MF Mulcahy, EB Durbin, AA Kulkarni, HH Nelson, S Shah, RP Rosovsky, K Reynolds, A Bardia, G Boland, J Gainor, L Zubiri, TR Halfdanarson, T Bekaii-Saab, A Desai, RA Mesa, M Bonnen, D Mahadevan, AG Ramirez, M Salazar, R Belenkaya, J Philip, GJ Riely, B Faller, RR McKay, A Ajmera, A Cabal, JA Shaya, LB Weissmann, C Jani, JL Chen, ME Gatti-Mays, SR Jhawar, MB Lustberg, JD Palmer, C Pillainayagam, DG Stover, S Wall, NO Williams, V Karivedu, D Addison, M Joshi, H Menon, MA Rovito, A Elshoury, SK Jabbour, MR Shah, B Bashir, SZ Mahmood, C McNair, V Mico, AV Rivera, C Miller, E Cabebe, MJ Glover, A Jha, L Schapira, SA Shah, JT Wu, S Subbiah, BB Logan, G Kloecker, , K Russell, B Stith, M Smits, N Edwin, DD Chism, S Owenby, DB Doroshow, MD Galsky, H Zhu, JC Fu, A Fazio, KG Patel, J Riess, DH Kwon, V Kumar, JY Islam, WA Wood, SA Ahmad, P Grover, S Gulati, J Kharofa, M Marcum, C Park, TM Wise-Draper, DW Bowles, CL Geiger, R Bishnoi, MJ Markham, C Shah, JD Acoba, YS Rho, LE Feldman, KF Hoskins, G Gantt, M Khan, RH Nguyen, MM Pasquinelli, C Schwartz, NK Venepalli, P Vikas, A Kasi, LA Fecher, CR Friese, BH Mavromatis, QU Zaman, R Bijjula, A Cheng, EJ Davis, B French, EA Gillaspie, DJ Hausrath, C Hennessy, CY Hsu, DB Johnson, X Li, SA Reid, BI Rini, Y Shyr, DA Slosky, CC Solorzano, MD Tucker, K Vega-Luna, LL Wang, KT Enriquez, T Sun, TM Carducci, M Puc, SV Loon, KJ Goldsmith, RL Rice, WD Cabalona, C Pilar, BB McCollough, P Peddi, LR Rosen, MA Bilen, D Ravindranathan, N Hafez, RS Herbst, P LoRusso, T Masters, C Stratton
JAMA Oncology 2021
Outcomes of COVID-19 in Patients With Cancer: A Closer Look at Pre-Emptive Routine Screening Strategies
Z Xie, AN Saliba, J Abeykoon, U Majeed, DR Almquist, JE Wiedmeier-Nutor, E Bezerra, X Andrade-Gonzalez, A Hickman, K Sorenson, S Rakshit, C Wee, SH Tella, A Kommalapati, N Abdallah, J Pritchett, MD Andrade, D Uprety, A Badley, R Manochakian, S Ailawadhi, AH Bryce, JM Hubbard, N Gangat, CA Thompson, TE Witzig, RR McWilliams, K Leventakos, TR Halfdanarson
2021
COVID-19 in immunocompromised populations: implications for prognosis and repurposing of immunotherapies
JD Goldman, PC Robinson, TS Uldrick, P Ljungman
Journal for ImmunoTherapy of Cancer 2021
Cardio-oncology Training in the COVID-19 Era
S Feldman, J Liu, R Steingart, D Gupta
Current Treatment Options in Oncology 2021
COVID-19 and stem cell transplantation; results from an EBMT and GETH multicenter prospective survey
P Ljungman, R de la Camara, M Mikulska, G Tridello, B Aguado, MA Zahrani, J Apperley, A Berceanu, RM Bofarull, M Calbacho, F Ciceri, L Lopez-Corral, C Crippa, ML Fox, A Grassi, MJ Jimenez, SK Demir, M Kwon, CV Llamas, JL Lorenzo, S Mielke, K Orchard, RP Porras, D Vallisa, A Xhaard, NS Knelange, A Cedillo, N Kröger, JL Piñana, J Styczynski
Leukemia 2021
Personalized at-home autologous hematopoietic stem cell transplantation during the SARS-CoV-2 outbreak
A Martínez-Roca, LG Rodríguez-Lobato, N Ballestar, C Gallego, F Fernández-Avilés
Leukemia Research 2021
Aseptic Meningitis after Recovery from SARS-CoV-2 in an Allogeneic Stem Cell Transplant Recipient
F Basher, JF Camargo, M Diaz-Paez, LJ Lekakis, DL Pereira
Clinical medicine insights. Case reports 2021
Clinical course and outcomes of COVID‐19 in hematopoietic cell transplant patients, a regional report from the Middle East
RE Fakih, A Haroon, F Alfraih, MK Al-Khabori, M Alzahrani, A Alhuraiji, A Hamadah, NI AlJohani, B Alahmari, MF Essa, IH Motabi, IK Tailor, RS Almaghrabi, K Al-Farsi, I Abosoudah, M Ayas, TA Elhassan, AM Suhebeh, SO Ahmed, S Alhayli, P Kaloyannidis, A Alsaeed, KA Anezi, S Alamoudi, M Damlaj, HA Hashmi, M Aljurf
Bone Marrow Transplantation 2021
Clinical presentation and outcomes of COVID‐19 following hematopoietic cell transplantation and cellular therapy
JF Camargo, MA Mendoza, R Lin, IV Moroz, AD Anderson, MI Morris, Y Natori, A Natori, M Raja, L Lekakis, A Beitinjaneh, A Jimenez, M Goodman, T Wang, KV Komanduri, D Pereira
Transplant Infectious Disease 2021
COVID-19 and Hematopoietic Cell Transplantation Center-Specific Survival Analysis: Can We Adjust for the Impact of the Pandemic? Recommendations of the COVID-19 Task Force of the 2020 Center for International Blood and Marrow Transplantation Research Center Outcomes Forum
JR Wingard, KW Ahn, C Dandoy, MA Perales, WA Wood, B Logan, M Riches, JD Rizzo
2021
COVID-19 vaccines for patients with haematological conditions
C Sun, C Pleyer, A Wiestner
The Lancet Haematology 2021
Risk factors for seasonal human coronavirus lower respiratory tract infection after hematopoietic cell transplantation
C Ogimi, H Xie, A Waghmare, MU Oshima, KK Mallhi, KR Jerome, WM Leisenring, JA Englund, M Boeckh
Blood Advances 2021
Immune reconstitution and severity of COVID‐19 among hematopoietic cell transplant recipients
AE Malek, JA Adachi, VE Mulanovich, J Sassine, II Raad, K McConn, GT Seiler, U Dhal, F Khawaja, RF Chemaly
Transplant Infectious Disease 2021
Cellular Therapy During COVID-19: Lessons Learned and Preparing for Subsequent Waves
MT Nawas, GL Shah, DR Feldman, JD Ruiz, EV Robilotti, AA Aslam, M Dundas, M Kamboj, JN Barker, C Cho, DJ Chung, PB Dahi, SA Giralt, B Gyurkocza, OB Lahoud, HJ Landau, RJ Lin, S Mailankody, ML Palomba, EB Papadopoulos, I Politikos, DM Ponce, CS Sauter, BC Shaffer, M Scordo, MR van den Brink, MA Perales, R Tamari
2021
Oncologic immunomodulatory agents in patients with cancer and COVID-19
J Jee, AJ Stonestrom, S Devlin, T Nguyentran, B Wills, V Narendra, MB Foote, M Lumish, SA Vardhana, SM Pastores, N Korde, D Patel, S Horwitz, M Scordo, AF Daniyan
Scientific Reports 2021
Case Discussion and Literature Review: Cancer Immunotherapy, Severe Immune-Related Adverse Events, Multi-Inflammatory Syndrome, and Severe Acute Respiratory Syndrome Coronavirus 2
D Ragoonanan, SJ Khazal, R Mejia, L Ewing, JB Durand, L Bashoura, J Tayar, ND Garnes, D Petropoulos, P Tewari, M Bhatti, AH Ahmad, J Cortes, S Razvi, K McBeth, R Swinford, B Shoberu, W Waseemuddin, L Chi, JB Gill, W Zaky, N Daw, C Gutierrez, W Tereffe, P Kebriaei, K Rezvani, EJ Shpall, RE Champlin, KM Mahadeo
Frontiers in Oncology 2021
Use of Telehealth for Domiciliary Follow-up After Hematopoietic Cell Transplantation During the COVID-19 Pandemic: Prospective Pilot Study
A Mussetti, MQ Salas, M Condom, M Antonio, C Ochoa, I Ivan, DJ la Torre, GS Linares, B Ansoleaga, B Patiño-Gutierrez, L Jimenez-Prat, R Parody, A Sureda-Balari
2021
Clinical characteristics and outcomes of COVID-19 in haematopoietic stem-cell transplantation recipients: an observational cohort study
A Sharma, NS Bhatt, AS Martin, MB Abid, J Bloomquist, RF Chemaly, C Dandoy, J Gauthier, L Gowda, MA Perales, S Seropian, BE Shaw, EE Tuschl, AM Zeidan, ML Riches, GL Shah
The Lancet Haematology 2021
CD19+IgD+CD27- Naïve B Cells as Predictors of Humoral Response to COVID 19 mRNA Vaccination in Immunocompromised Patients
E Schulz, I Hodl, P Forstner, S Hatzl, N Sareban, M Moritz, J Fessler, B Dreo, B Uhl, C Url, AJ Grisold, M Khalil, B Kleinhappl, C Enzinger, MH Stradner, HT Greinix, P Schlenke, I Steinmetz
Frontiers in immunology 2021
Coronavirus disease 2019 in immunocompromised patients: a comprehensive review of coronavirus disease 2019 in hematopoietic stem cell recipients
A Lafarge, A Mabrouki, E Yvin, S Bredin, Y Binois, R Clere-Jehl, E Azoulay
Current Opinion in Critical Care 2021
MIS-C clinical guidance released amid race to define the condition
J Clarke
Nature Reviews Rheumatology 2020
COVID-19—Lessons Learned and Questions Remaining
FC Fang, CA Benson, C del Rio, KM Edwards, VG Fowler, DN Fredricks, AP Limaye, BE Murray, S Naggie, PG Pappas, R Patel, DL Paterson, DA Pegues, WA Petri, RT Schooley
Clinical Infectious Diseases 2020
Expanding the toolbox to combat a pandemic
SE Prockop
Blood 2020
Complications after CD19+ CAR T-Cell Therapy
O Penack, C Koenecke
Cancers 2020
Humoral serologic response to the BNT162b2 vaccine is abrogated in lymphoma patients within the first 12 months following treatment with anti-CD2O antibodies
R Gurion, U Rozovski, G Itchaki, A Gafter-Gvili, C Leibovitch, P Raanani, H Ben-Zvi, M Szwarcwort, M Taylor-Abigadol, E Dann, N Horesh, T Inbar, I Tzoran, N Lavi, R Fineman, S Ringelstein-Harlev, N Horowitz
Haematologica 2020

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