BMJ Open (Apr 2022)

Impact of the COVID-19 pandemic on patients with paediatric cancer in low-income, middle-income and high-income countries: a multicentre, international, observational cohort study

  • ,
  • Mohamed Ahmed,
  • Ahmad Mansour,
  • Ahmed Samir,
  • Charlotte Smith,
  • Lubna Samad,
  • Vaishnavi Govind,
  • Fakher Rahim,
  • Augusto Zani,
  • Muhammad Arshad,
  • Sadaf Altaf,
  • Chan Hon Chui,
  • Pooja Kumari,
  • Thomas Smith,
  • Ayesha Saleem,
  • Darica Au,
  • Kate Cross,
  • Kokila Lakhoo,
  • Anna Maria Testi,
  • Robyn Brown,
  • Noel Peter,
  • Francesco Pata,
  • Adesoji Ademuyiwa,
  • Tahmina Banu,
  • Bruce Bvulani,
  • Milind Chitnis,
  • Maryam Ghavami Adel,
  • Matthew H V Byrne,
  • Pierfrancesco Lapolla,
  • Andrea Mingoli,
  • Lucy Davies,
  • Dennis Mazingi,
  • Hamidah Alias,
  • Simone de Campos Vieira Abib,
  • Ibukunolu Olufemi Ogundele,
  • Laila Hessissen,
  • Mohammad Ahmad,
  • Maricarmen Olivos,
  • Daniel Rhee,
  • Maryam Khan,
  • Christine Nitschke,
  • Alexandra Valetopoulou,
  • Ashrarur Rahman Mitul,
  • Sabbir Karim,
  • Gaetano Gallo,
  • Mohamedraed Elshami,
  • Mahmoud Elfiky,
  • Soham Bandyopadhyay,
  • Muath Alser,
  • Elliott H Taylor,
  • Duha Jasim,
  • Somy Charuvila,
  • Nazmul Islam,
  • William B Lo,
  • Robin Simpson,
  • Zarina Abdul Latiff,
  • Bruno Cirillo,
  • Gioia Brachini,
  • Megan Murphy,
  • Zineb Bentounsi,
  • Anette S Jacobsen,
  • Anna Casey,
  • Abdulrasheed A Nasir,
  • Taiwo Akeem Lawal,
  • Samson Olori,
  • Michael Boettcher,
  • Muhammed Elhadi,
  • Shaun Wilson,
  • Dragana Janić,
  • Patricia Shinondo,
  • Shireen Anne Nah,
  • Alhassan Abdul-Mumin,
  • Dayang Anita Abdul Aziz,
  • J Benjamin,
  • Karl-Heinz Frosch,
  • Poorvaprabha Patil,
  • Sarah Muma,
  • Emmanuel Uwiringiyimana,
  • Athanasios Tragiannidis,
  • Mahan Salehi,
  • Sara Ali,
  • Hafeez Abdelhafeez,
  • Max Pachl,
  • Benjamin Martin,
  • Sonal Nagras,
  • Mihir Sheth,
  • Catherine Dominic,
  • Suraj Gandhi,
  • Divya Parwani,
  • Rhea Raj,
  • Diella Munezero,
  • Rohini Dutta,
  • Nsimire Mulanga Roseline,
  • Kellie McClafferty,
  • Armin Nazari,
  • Smrithi Sriram,
  • Sai Pillarisetti,
  • Aishwarya Ashwinee,
  • Gul Kalra,
  • Priyansh Nathani,
  • Khushman Kaur Bhullar,
  • Nehal Rahim,
  • Shweta Madhusudanan,
  • Joshua Erhabor,
  • Manasi Shirke,
  • Aishah Mughal,
  • Sravani Royyuru,
  • Daniel Robinson,
  • Mehdi Khan,
  • Alexandre Dukundane,
  • Kwizera Festus,
  • Rohan Pancharatnam,
  • Lorraine Ochieng,
  • Hritik Nautiyal,
  • Leanne Gentle,
  • Ehab Hanafy,
  • Catherine Yang,
  • John Mathew,
  • Olumide Abiodun Elebute,
  • Oluwaseun Ladipo-Ajayi,
  • Okechukwu Hyginus Ekwunife,
  • Sherief Ghozy,
  • Aya Zazo,
  • Salah Eddine Oussama Kacimi,
  • Ahmed Sherif,
  • Krithi Ravi,
  • Nermin Badwi,
  • Hajar Moujtahid,
  • Ariana Axiaq,
  • Eman Abdulwahed,
  • Kemal Tolga Saracoglu,
  • Yasin Kara,
  • Ahmed Y Azzam,
  • Omar Elmandouh,
  • Simone de Campos Vieira Abib,
  • KingDavid Nweze,
  • Syeda Namayah Fatima Hussain,
  • Marta de Andres Crespo,
  • Fatumata Jalloh,
  • Shahnur Shah,
  • Rohini Rajpal,
  • Masooma Rana,
  • Muskaan Abdul Qadir,
  • Abdelrahman Azzam,
  • Mayara Fanelli,
  • Gustavo Mendonça Ataíde Gomes,
  • Igor Lima Buarque,
  • Isadora Schwaab Guerini,
  • Anfel Bouderbala,
  • Sarah Alfurais,
  • Mohamed Gamal,
  • Yara Hijazi,
  • Shatha Tailakh,
  • Hamza AlNaggar,
  • Zain Douba,
  • Sewar Elejla,
  • Abdullah Eldaly,
  • Ekram Sharashi,
  • Tamara Elyan,
  • Aouabed Nesrine,
  • Ammar Ayman,
  • Mohamed Bonna,
  • Safia Lorabi,
  • Hassan Alalami,
  • Rawan Yasser Emam,
  • Mohamad K Abou Chaar,
  • Hira Zuberi,
  • Iyad Sultan,
  • Dhruv Nath Ghosh,
  • Nitin James Peters,
  • Reto M Baertschiger,
  • Kefas John Bwala,
  • AM Umar,
  • Abdurahaman Aremu,
  • Dauda E Suleiman,
  • Tybat Aliyu,
  • Kashaf Turk,
  • Oluseyi Oyebode Ogunsua,
  • Tunde Talib Sholadoye,
  • Musliu Adetola Tolani,
  • Yakubu Alfa,
  • Keffi Mubarak Musa,
  • Mwangi Irungu,
  • Ken Muma,
  • Mitchelle Obat,
  • Youssef Sameh Badran,
  • Abdulrahman Ghassan Qasem,
  • Faris Ayasra,
  • Reema Alnajjar,
  • Mohamed Abdel-Maboud,
  • Abdelrahman Bahaa,
  • Ayat M Saadeldin,
  • Mohamed Adwi,
  • Mahmoud Adly,
  • Abdallah Elshenawy,
  • Amer Harky,
  • Kirstie Wright,
  • Jessica Luyt,
  • Olivia White,
  • Nathan Thompson,
  • Imogen Harrison,
  • Sara Kader Alsaeiti,
  • Fatma Saleh Benkhial,
  • Mohammed Miftah Faraj Almihashhish,
  • Eman Salem Muftah Burzeiza,
  • Raja Mari Mohammed Nasef,
  • Hend Mohammed Masoud,
  • Mabroukah Saeid Alshamikh,
  • Fatma Mohammed Masoud,
  • Nyararai Togarepi,
  • Elaine Carrolan,
  • Mohamed Hassanin O'Sullivan,
  • Ahmed Saleh,
  • Mahmoud Bassiony,
  • Mostafa Qatora,
  • Mohamed Bahaaeldin,
  • Shady Fadel,
  • Yasmine El Chazli,
  • Kamel Hamizi,
  • Mehdi Anouar Zekkour,
  • Rima Rahmoun,
  • Boutheyna Drid,
  • Salma Naje Abu Teir,
  • Mohamed Yazid Kadir,
  • Yassine Zerizer,
  • Nacer Khernane,
  • Brahim Saada,
  • Imane Ammouze,
  • Yahya Elkaoune,
  • Ghita Chaoui,
  • Hajar Benaouda,
  • Meryem Gounni,
  • Narjiss Aji,
  • Joana Mafalda Monteiro,
  • Susana Nunes,
  • Maria do Bom-Sucesso,
  • Dave R. Lal,
  • Brian T. Craig,
  • Kerri Becktell,
  • Md Afruzul Alam,
  • Orindom Shing Pulock,
  • Tasmiah Tahera Aziz,
  • Rosanda Ilic,
  • Danica Grujicic,
  • Tijana Nastasovic,
  • Igor Lazic,
  • Mihailo Milicevic,
  • Vladimir Bascarevic,
  • Radovan Mijalcic,
  • Vuk Scepanovic,
  • Aleksandar Stanimirovic,
  • Aleksandra Paunovic,
  • Ivan Bogdanovic,
  • Shahnoor Islam,
  • AKM Amirul Morshed,
  • A. K. M. Khairul Basher,
  • Mehnaz Akter,
  • S. M. Rezanur Rahman,
  • Zannat Ara,
  • Mohammed Tanvir Ahammed,
  • Tania Akter,
  • Kamrun Nahar,
  • Fatema Sayed,
  • Ashfaque Nabi,
  • Md. Asif Iqbal,
  • Md. Masud Rana,
  • Md. Asaduzzaman,
  • Md. Hasanuzzaman,
  • Elif Akova,
  • Evren Aydogmus,
  • Bekir Can Kendirlioglu,
  • Tufan Hicdonmez,
  • Arshiya Adhnon,
  • Asim Noor Rana,
  • Hani Humad,
  • Anjan Madasu,
  • Mohammed A Azab,
  • Alzhraa Salah Abbas,
  • Olanrewaju Moses,
  • Ibiyeye Taiye Taibat,
  • Taiwo Jones,
  • Kalu Ukoha,
  • Olagundoye Goke,
  • Okorie Ikechukwu,
  • Abiodun Idowu Okunlola,
  • Helga Nauhaus,
  • Danelle Erwee,
  • Agata Chylinska,
  • Prasanna Gomes,
  • Marco Aurelio Ciriaco Padilha,
  • Elvercio Pereira de Oliveira Junior,
  • Lucas Garschagen de Carvalho,
  • Fabiola Leonelli Diz,
  • Mohamed El Kassas,
  • Usama Eldaly,
  • Ahmed Tawheed,
  • Mohamed Abdelwahab,
  • Oudrhiri Mohammed Yassaad,
  • Bechri Hajar,
  • El Ouahabi Abdessamad,
  • Arkha Yasser,
  • Hessissen Laila,
  • Farah Sameer Yahya,
  • Yasir Al-Agele,
  • Maria Teresa Peña Gallardo,
  • Jacqueline Elizabeth Montoya Vásquez,
  • Juan Luis García León,
  • Sebastián Shu Yip,
  • Mariam Lami,
  • Harmit Ghattaura,
  • Eric W Etchill,
  • Stacy Cooper,
  • Kevin Crow,
  • Morgan Drucker,
  • Benjamin Shou,
  • Alan Siegel,
  • Gül Nihal Özdemir,
  • Ehab El Refaee,
  • John George Massoud,
  • Ayah Bassam Ibrahim,
  • Ruaa Bassam Ibrahim,
  • Faris Abu Za'nouneh,
  • Ranya M. Baddourah,
  • Toqa Fahmawee,
  • Ayah Al_Shraideh,
  • Ghazwani Salman,
  • Ehab Alameer,
  • Al-Mudeer Ali,
  • Ghazwani Yahia,
  • Khozairi Waleed,
  • Mohamad K. Abou Chaar,
  • Khalil Ghandour,
  • Shaima' Al-Dabaibeh,
  • Ammar Al-Basiti,
  • Hazim Ababneh,
  • Omaima El-Qurneh,
  • Yousef Alalawi,
  • Ahmad Al Ayed,
  • Naif Al Bolowi,
  • Amos HP Loh,
  • Heidi Barola,
  • Aubrey L Pagaduan,
  • Jingdan Fan,
  • Adesoji O. Ademuyiwa,
  • Christopher O. Bode,
  • Justina O. Seyi-Olajide,
  • Felix M. Alakaloko,
  • George C. Ihediwa,
  • Kareem O. Musa,
  • Edamisan O. Temiye,
  • Olufemi Oni,
  • Adeseye M. Akinsete,
  • Janita Zarrish,
  • Ramsha Saleem,
  • Soha Zahid,
  • Atiqa Amirali,
  • Ahsan Nadeem,
  • Sameer Saleem Tebha,
  • Zonaira Qayyum,
  • Sana Tahir,
  • Anneqa Tahir,
  • Rabbey Raza Khan,
  • Ayesha Mehmood,
  • Taimur Iftikhar Qureshi,
  • Victor Calvagna,
  • Nathalie Galea,
  • Matthew R Schuelke,
  • Jake A. Kloebe,
  • Robert L. Owen,
  • Alexander S. Roth,
  • J. Hudson Barnett,
  • Lucien P. Jay,
  • Kirk David Wyatt,
  • Paul J. Galardy,
  • Agnes Vojcek,
  • Mahmoud Maher Abdelnaby Alrahawy,
  • Seham M Ragab,
  • Abdallah R Allam,
  • Eman Ibrahim Hager,
  • Kıvılcım Karadeniz Cerit,
  • Adnan Dağçınar,
  • Tümay Umuroğlu,
  • Ayten Saraçoğlu,
  • Mustafa Sakar,
  • Can Kıvrak,
  • Gül Çakmak,
  • Ibrahim Sallam,
  • Gamal Amira,
  • Mohamed Sherief,
  • Simone de Oliveira Coelho,
  • Arissa Ikeda,
  • Licia Portela,
  • Marianne Monteiro Garrigo,
  • Ricardo Vianna de Carvalho,
  • Fernanda Lobo,
  • Sima Ester Ferman,
  • Fernanda Ferreira da Silva Lima,
  • Moawia Mohammed Ali Elhassan,
  • Nada Osman Yousif Elhaj,
  • Hytham K. S. Hamid,
  • Emmanuel A. Ameh,
  • Vincent E. Nwatah,
  • Adewumi B. Oyesakin,
  • Andrew Nwankwo Osuigwe,
  • Chisom Adaobi Nri-Ezedi,
  • Eric Okechukwu Umeh,
  • Nellie Patiala,
  • Abiodun Folashade Adekanmbi,
  • Olubunmi Motunrayo Fatungase,
  • Olubunmi Obafemi Obadaini,
  • Sarah Al-Furais,
  • Humaida Hemlae,
  • Sreylis Nay,
  • R M Jeffri Ismail,
  • Simonede Campos Vieira Abib,
  • Fabianne Altruda de Moraes Costa Carlesse,
  • Mayara Caroline Amorim Fanelli,
  • Fernanda Kelly Marques de Souza,
  • Denis Cozzi,
  • Paolo Musiu,
  • Paolo Sapienza,
  • Martina Zambon,
  • Simona Meneghini,
  • Pierfranco Cicerchia,
  • Abdulrahman Omar Taha,
  • Bouaoud Souad,
  • Mebarki Malika,
  • Bioud Belkacem,
  • Ayman Meelad,
  • Hajier Salim Alrashed,
  • Fayza Haider,
  • Fatema Naser Al Fayez,
  • Halwani Yaninga Fuseini,
  • Peter Gyamfi Kwarteng,
  • Abubakari Bawa Abdulai,
  • Sheba Mary Pognaa Kunfah,
  • Gilbert B. Bonsaana,
  • Stephanie Ajinkpang,
  • Edmund M. Der,
  • Francis A. Abantanga,
  • Mary Joan Kpiniong,
  • Kingsley Aseye Hattor,
  • Kingsley Appiah Bimpong,
  • Mohamed Elbahnasawy,
  • Sherief Abdelsalam,
  • Reto M. Baertschiger,
  • Amanpreet Brar,
  • Andreea C Matei,
  • Hira Khalid Zuberi,
  • Kishwer Nadeem,
  • Naema Khayyam,
  • Fatima Ambreen Imran,
  • Nida Zia,
  • Sadia Muhammad,
  • Muhammad Rafie Raza,
  • Muhammad Rahil Khan,
  • Alaa Hamdan,
  • Abdeljawad Mazloum,
  • Ali Abodest,
  • Nisreen Ali,
  • Bardisan Gawarieh,
  • Ammar Omran,
  • Almed Moussa,
  • Alaa Ahmed,
  • Munawar Hraib,
  • Victor Khoury,
  • Abdulrahman Almjersah,
  • Mohammad Ali Deeb,
  • Almahmod Alkhalil,
  • Akram Ahmed,
  • Ali Alelayan,
  • Ali Hammed,
  • Wassem Shater,
  • Ahmad Bouhuwaish,
  • Alqasim Abdulkarim,
  • Marwa Biala,
  • Reem Ghamgh,
  • Amani Alamre,
  • Marwa Shelft,
  • Asmaa A. M. Albanna,
  • Hoda Tawel,
  • Emmanuel Hatzipantelis,
  • Eleni Tsotridou,
  • Assimina Galli-Tsinopoulou,
  • C-Khai Loh,
  • Doris Lau,
  • Azrina Syarizad Khutubul,
  • Raphael N. Vuille-dit-Bille,
  • Stefan G. Holland-Cunz,
  • Nima Allafi,
  • Kelvin Ifeanyichukwu Egbuchulem,
  • Olakayode Olaolu Ogundoyin,
  • Isaac Dare Olulana,
  • Biobele J. Brown,
  • Oluwasegun Joshua Afolaranmi,
  • AbdulBasit Fehintola,
  • Annika Heuer,
  • Matthias Priemel,
  • Lennart Viezens,
  • Martin Stangenberg,
  • Marc Dreimann,
  • Alonja Reiter,
  • Jasmin Meyer,
  • Leon Köpke,
  • Uduak Offiong,
  • Philip Mari Mshelbwala,
  • Fashie Andrew Patrick,
  • Aminu Muhammed Umar,
  • N Otene ThankGod,
  • Kazeem O. O. Ibrahim,
  • Dupe S. Ademola-Popoola,
  • Olayinka T. Sayomi,
  • Alege Abdurrzzaq,
  • Ademola A. Adeyeye,
  • Khadijah O. Omokanye,
  • Lukman O Abdur-Rahman,
  • Olubisi Olutosin Bamidele,
  • Shakirullah AbdulAzeez,
  • Aminat Akinoso,
  • Michael O. Adegboye,
  • Yuki Julius Ng,
  • Syukri Ahmad Zubaidi,
  • Murad Almasri,
  • Rasaq Olaosebikan,
  • Akila Muthukumar,
  • Amon Ngongola,
  • Azad Patel,
  • Abdullahi Nuhu-Koko,
  • Baba Jibrin,
  • Ajiboye L. Olalekan,
  • Christopher S. Lukong,
  • Ezekiel I. Ajayi,
  • Gabriela Guillén,
  • Sergio López,
  • José Andrés Molino,
  • Pablo Velasco,
  • Omar Hamam,
  • Rim Elmandouh,
  • Nensi Melissa Ruzgar,
  • Rachel Levinson,
  • Shashwat Kala,
  • Sarah Ullrich,
  • Emily Christison-Lagay,
  • Aya Sabry Mortada,
  • Mahmoud Ahmed Ebada,
  • Eman Seif Alnaser Solimam,
  • Khaled Abualkher,
  • Amr Mohammed Elsayed Yousf,
  • Mohamed Mohamed Holail,
  • Reem Mohamed Almowafy,
  • Janice Hui Ling Wong,
  • Reto Baertschiger,
  • Essam Elhalaby,
  • Mahmoud M. Saad,
  • Guido Seitz,
  • Judith Lindbert,
  • Francis Abantanga Georgios Tsoulfas,
  • Asimina Galli-Tsinopoulou,
  • Calogero Virgone,
  • Mohammad K. Abou Chaar,
  • Eric Mwangi Irungu,
  • Outani Oumaima,
  • Dhruv Nath Ghosh,
  • Lily Saldana,
  • Jan Godzinsky,
  • Abdelbasit Ali,
  • Mohamed Bella Jalloh,
  • Nellie Bell,
  • Annette Jacobsen,
  • Israel Fernandez Pineda,
  • Lucas Krauel,
  • Waha Rahama,
  • Hazim Elfatih,
  • Arda Isik,
  • Andrea Hayes-Jordan,
  • Roshni Dasgupta

DOI
https://doi.org/10.1136/bmjopen-2021-054690
Journal volume & issue
Vol. 12, no. 4

Abstract

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Objectives Paediatric cancer is a leading cause of death for children. Children in low-income and middle-income countries (LMICs) were four times more likely to die than children in high-income countries (HICs). This study aimed to test the hypothesis that the COVID-19 pandemic had affected the delivery of healthcare services worldwide, and exacerbated the disparity in paediatric cancer outcomes between LMICs and HICs.Design A multicentre, international, collaborative cohort study.Setting 91 hospitals and cancer centres in 39 countries providing cancer treatment to paediatric patients between March and December 2020.Participants Patients were included if they were under the age of 18 years, and newly diagnosed with or undergoing active cancer treatment for Acute lymphoblastic leukaemia, non-Hodgkin’s lymphoma, Hodgkin lymphoma, Wilms’ tumour, sarcoma, retinoblastoma, gliomas, medulloblastomas or neuroblastomas, in keeping with the WHO Global Initiative for Childhood Cancer.Main outcome measure All-cause mortality at 30 days and 90 days.Results 1660 patients were recruited. 219 children had changes to their treatment due to the pandemic. Patients in LMICs were primarily affected (n=182/219, 83.1%). Relative to patients with paediatric cancer in HICs, patients with paediatric cancer in LMICs had 12.1 (95% CI 2.93 to 50.3) and 7.9 (95% CI 3.2 to 19.7) times the odds of death at 30 days and 90 days, respectively, after presentation during the COVID-19 pandemic (p<0.001). After adjusting for confounders, patients with paediatric cancer in LMICs had 15.6 (95% CI 3.7 to 65.8) times the odds of death at 30 days (p<0.001).Conclusions The COVID-19 pandemic has affected paediatric oncology service provision. It has disproportionately affected patients in LMICs, highlighting and compounding existing disparities in healthcare systems globally that need addressing urgently. However, many patients with paediatric cancer continued to receive their normal standard of care. This speaks to the adaptability and resilience of healthcare systems and healthcare workers globally.