Observational Study

. 2021 Dec;6(4):542-552.

doi: 10.1136/svn-2020-000695. Epub 2021 Mar 26.

Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic

Thanh N Nguyen^#¹, Diogo C Haussen², Muhammad M Qureshi³, Hiroshi Yamagami⁴, Toshiyuki Fujinaka⁵, Ossama Y Mansour⁶, Mohamad Abdalkader⁷, Michael Frankel², Zhongming Qiu⁸, Allan Taylor⁹, Pedro Lylyk¹⁰, Omer F Eker¹¹, Laura Mechtouff¹², Michel Piotin¹³, Fabricio Oliveira Lima¹⁴, Francisco Mont'Alverne¹⁵, Wazim Izzath¹⁶, Nobuyuki Sakai¹⁷, Mahmoud Mohammaden², Alhamza R Al-Bayati², Leonardo Renieri¹⁸, Salvatore Mangiafico¹⁸, David Ozretic¹⁹, Vanessa Chalumeau²⁰, Saima Ahmad²¹, Umair Rashid²¹, Syed Irteza Hussain²², Seby John²², Emma Griffin²³, John Thornton²³, Jose Antonio Fiorot²⁴, Rodrigo Rivera²⁵, Nadia Hammami²⁶, Anna M Cervantes-Arslanian²⁷, Hormuzdiyar H Dasenbrock²⁸, Huynh Le Vu²⁹, Viet Quy Nguyen²⁹, Steven Hetts^{30

31}, Romain Bourcier³², Romain Guile³², Melanie Walker³³, Malveeka Sharma³⁴, Don Frei³⁵, Pascal Jabbour³⁶, Nabeel Herial³⁶, Fawaz Al-Mufti³⁷, Atilla Ozcan Ozdemir³⁸, Ozlem Aykac³⁸, Dheeraj Gandhi³⁹, Chandril Chugh⁴⁰, Charles Matouk⁴¹, Pascale Lavoie⁴², Randall Edgell⁴³, Andre Beer-Furlan⁴⁴, Michael Chen⁴⁴, Monika Killer-Oberpfalzer⁴⁵, Vitor Mendes Pereira⁴⁶, Patrick Nicholson⁴⁶, Vikram Huded⁴⁷, Nobuyuki Ohara⁴⁸, Daisuke Watanabe⁴⁹, Dong Hun Shin⁵⁰, Pedro Sc Magalhaes⁵¹, Raghid Kikano⁵², Santiago Ortega-Gutierrez⁵³, Mudassir Farooqui⁵³, Amal Abou-Hamden⁵⁴, Tatsuo Amano⁵⁵, Ryoo Yamamoto⁵⁶, Adrienne Weeks⁵⁷, Elena A Cora⁵⁸, Rotem Sivan-Hoffmann⁵⁹, Roberto Crosa⁶⁰, Markus Möhlenbruch⁶¹, Simon Nagel⁶², Hosam Al-Jehani⁶³, Sunil A Sheth⁶⁴, Victor S Lopez Rivera⁶⁴, James E Siegler⁶⁵, Achmad Fidaus Sani⁶⁶, Ajit S Puri⁶⁷, Anna Luisa Kuhn⁶⁷, Gianmarco Bernava⁶⁸, Paolo Machi⁶⁸, Daniel G Abud⁶⁹, Octavio M Pontes-Neto⁷⁰, Ajay K Wakhloo⁷¹, Barbara Voetsch⁷², Eytan Raz⁷³, Shadi Yaghi⁷⁴, Brijesh P Mehta⁷⁵, Naoto Kimura⁷⁶, Mamoru Murakami⁷⁷, Jin Soo Lee⁷⁸, Ji Man Hong⁷⁸, Robert Fahed⁷⁹, Gregory Walker⁷⁹, Eiji Hagashi⁸⁰, Steve M Cordina⁸¹, Hong Gee Roh⁸², Ken Wong⁸³, Juan F Arenillas⁸⁴, Mario Martinez-Galdamez⁸⁵, Jordi Blasco⁸⁶, Alejandro Rodriguez Vasquez⁸⁷, Luisa Fonseca⁸⁸, M Luis Silva⁸⁹, Teddy Y Wu⁹⁰, Simon John⁹¹, Alex Brehm⁹², Marios Psychogios⁹², William J Mack⁹³, Matthew Tenser⁹³, Tatemi Todaka⁹⁴, Miki Fujimura⁹⁵, Roberta Novakovic⁹⁶, Jun Deguchi⁹⁷, Yuri Sugiura⁹⁸, Hiroshi Tokimura⁹⁹, Rakesh Khatri¹⁰⁰, Michael Kelly¹⁰¹, Lissa Peeling¹⁰¹, Yuichi Murayama¹⁰², Hugh Stephen Winters¹⁰³, Johnny Wong¹⁰⁴, Mohamed Teleb¹⁰⁵, Jeremy Payne¹⁰⁵, Hiroki Fukuda¹⁰⁶, Kosuke Miyake¹⁰⁷, Junsuke Shimbo¹⁰⁸, Yusuke Sugimura¹⁰⁹, Masaaki Uno¹¹⁰, Yohei Takenobu¹¹¹, Yuji Matsumaru¹¹², Satoshi Yamada¹¹³, Ryuhei Kono¹¹⁴, Takuya Kanamaru¹¹⁵, Masafumi Morimoto¹¹⁶, Junichi Iida¹¹⁷, Vasu Saini¹¹⁸, Dileep Yavagal¹¹⁸, Saif Bushnaq¹¹⁹, Wenguo Huang¹²⁰, Italo Linfante¹²¹, Jawad Kirmani¹²², David S Liebeskind¹²³, Viktor Szeder¹²⁴, Ruchir Shah¹²⁵, Thomas G Devlin¹²⁵, Lee Birnbaum¹²⁶, Jun Luo¹²⁷, Anchalee Churojana¹²⁸, Hesham E Masoud¹²⁹, Carlos Ynigo Lopez¹²⁹, Brendan Steinfort¹³⁰, Alice Ma¹³⁰, Ameer E Hassan¹³¹, Amal Al Hashmi¹³², Mollie McDermott¹³³, Maxim Mokin¹³⁴, Alex Chebl¹³⁵, Odysseas Kargiotis¹³⁶, Georgios Tsivgoulis¹³⁷, Jane G Morris¹³⁸, Clifford J Eskey¹³⁹, Jesse Thon⁶⁵, Leticia Rebello¹⁴⁰, Dorothea Altschul¹⁴¹, Oriana Cornett¹⁴², Varsha Singh¹⁴², Jeyaraj Pandian¹⁴³, Anirudh Kulkarni¹⁴³, Pablo M Lavados¹⁴⁴, Veronica V Olavarria¹⁴⁴, Kenichi Todo¹⁴⁵, Yuki Yamamoto¹⁴⁶, Gisele Sampaio Silva¹⁴⁷, Serdar Geyik¹⁴⁸, Jasmine Johann³⁵, Sumeet Multani¹⁴⁹, Artem Kaliaev⁷, Kazutaka Sonoda¹⁵⁰, Hiroyuki Hashimoto¹⁵¹, Adel Alhazzani¹⁵², David Y Chung²⁷, Stephan A Mayer³⁷, Johanna T Fifi¹⁵³, Michael D Hill¹⁵⁴, Hao Zhang¹⁵⁵, Zhengzhou Yuan¹⁵⁶, Xianjin Shang¹⁵⁷, Alicia C Castonguay¹⁵⁸, Rishi Gupta¹⁵⁹, Tudor G Jovin⁶⁵, Jean Raymond¹⁶⁰, Osama O Zaidat¹¹⁹, Raul G Nogueira^#¹⁶¹; SVIN COVID-19 Registry, the Middle East North Africa Stroke and Interventional Neurotherapies Organization (MENA-SINO); Japanese Society of Vascular and Interventional Neurology Society (JVIN)

Affiliations

¹ Neurology, Radiology, Boston Medical Center, Boston, Massachusetts, USA.
² Neurology, Marcus Stroke & Neuroscience Center, Grady Memorial Hospital, Emory University School of Medicine, Atlanta, GA, USA.
³ Radiology, Radiation Oncology, Boston University School of Medicine, Boston, Massachusetts, USA.
⁴ Neurology, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁵ Neurosurgery, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁶ Neurology, Alexandria University, Alexandria, Egypt.
⁷ Radiology, Boston Medical Center, Boston, Massachusetts, USA.
⁸ Department of Neurology, Xinqiao Hospital, Chongqing, China.
⁹ Neurosurgery, University of Cape Town, Rondebosch, Western Cape, South Africa.
¹⁰ Neurosurgery, Interventional Neuroradiology, Clinica La Sagrada Familia, Buenos Aires, Argentina.
¹¹ Neuroradiologie, Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France.
¹² Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France.
¹³ Interventional Neuroradiology, Fondation Ophtalmologique Adolphe de Rothschild, Paris, Île-de-France, France.
¹⁴ Neurology, Hospital Geral de Fortaleza, Fortaleza, Brazil.
¹⁵ Interventional Neuroradiology, Hospital Geral de Fortaleza, Fortaleza, Brazil.
¹⁶ Neuroradiology, Nottingham University Hospitals NHS Trust, Nottingham, UK.
¹⁷ Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
¹⁸ Interventional Neurovascular Unit, University Hospital Careggi, Firenze, Toscana, Italy.
¹⁹ Neuroradiology, University Hospital Centre Zagreb, Zagreb, Croatia.
²⁰ Interventional Neuroradiology, Hopital Bicetre, Le Kremlin-Bicetre, France.
²¹ Stroke and Interventional Neuroradiology, Lahore General Hospital, Lahore, Pakistan.
²² Neurological Institute, Cleveland Clinic Abu Dhabi, Abu Dhabi, UAE.
²³ Department of Radiology, Beaumont Hospital, Dublin, Ireland.
²⁴ Neurology, Stroke Unit, Hospital-Estadual Central, Vitoria, Brazil.
²⁵ Neuroradiology, Instituto de Neurocirugia Dr Asengo, Santiago, Chile.
²⁶ Interventional Neuroradiology, Institut National de Neurologie, Tunis, Tunisia.
²⁷ Neurology, Boston Medical Center, Boston, Massachusetts, USA.
²⁸ Neurosurgery, Boston Medical Center, Boston, MA, USA.
²⁹ Stroke Center, Hue Central Hospital, Hue, Thua Thien Hue, Vietnam.
³⁰ Radiology, University of California San Francisco, San Francisco, California, USA.
³¹ Interventional Neuroradiology, University of California San Francisco, San Francisco, California, USA.
³² Neuroradiologie Diagnostique et Interventionnelle, Hôpital Guillaume & René Laennec, CHU Nantes, Nantes, France.
³³ Neurological Surgery, University of Washington School of Medicine, Seattle, Washington, USA.
³⁴ Neurology, University of Washington School of Medicine, Seattle, Washington, USA.
³⁵ Radiology, Swedish Medical Center, Englewood, Colorado, USA.
³⁶ Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, Pennsylvania, USA.
³⁷ Neurology, Neurosurgery, Westchester Medical Center Health Network, Valhalla, New York, USA.
³⁸ Stroke and Neurointervention Unit, Eskisehir OsmangaziUniversity, Eskisehir, Turkey.
³⁹ Radiology, Neurology, Neurosurgery, University of Maryland School of Medicine, Baltimore, Maryland, USA.
⁴⁰ Interventional Neurology, MAX Superspecialty Hospital, Saket, New Delhi, India.
⁴¹ Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA.
⁴² Neurosurgery, Centre Hospitalier Universitaire de Québec-Université Laval, Quebec, Quebec, Canada.
⁴³ Neurology, St Louis University School of Medicine, St Louis, Missouri, USA.
⁴⁴ Neurological Surgery, Rush University Medical Center, Chicago, IL, USA.
⁴⁵ Neurology, Research Institute of Neurointervention, University Hospital Salzburg /Paracelsus Medical University, Salzburg, Austria.
⁴⁶ Neurosurgery, Medical Imaging, Surgery, University of Toronto, Toronto, Ontario, Canada.
⁴⁷ Neurology, NH Mazumdar Shah Medical Center, Bangalore, India.
⁴⁸ Neurology, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
⁴⁹ Stroke and Neurovascular Surgery, IMS Tokyo-Katsushika General Hospital, Tokyo, Japan.
⁵⁰ Gachon University, Seongnam, Korea (the Republic of).
⁵¹ Stroke Unit, Hospital Municipal Sao Jose, Joinville, Santa Catarina, Brazil.
⁵² Interventional Neuroradiology, Lau Medical Center, Beirut, Lebanon.
⁵³ Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa, USA.
⁵⁴ Neurosurgery, Royal Adelaide Hospital, Adelaide, South Australia, Australia.
⁵⁵ Stroke and Cerebrovascular Medicine, Kyorin University, Mitaka, Tokyo, Japan.
⁵⁶ Neurology, Yokohama Brain and Spine Center, Yokohama, Japan.
⁵⁷ Neurosurgery, Dalhousie University, Halifax, Nova Scotia, Canada.
⁵⁸ Radiology, QEII Health Sciences Centre, Dalhousie University, Dalhousie, Nova Scotia, Canada.
⁵⁹ Interventional Neuroradiology, Rambam Health Care Campus, Haifa, Haifa, Israel.
⁶⁰ Centro Endovascular Neurologico Medica Uruguaya, Montevideo, Uruguay.
⁶¹ Neuroradiology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany.
⁶² Neurology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany.
⁶³ Neurosurgery, Interventional Radiology and Critical Care Medicine, King Fahad Hospital of the University, Imam Abdulrahman bin Faisal University, Alkhobar, Saudi Arabia.
⁶⁴ Neurology, University of Texas McGovern Medical School, Houston, Texas, USA.
⁶⁵ Neurology, Cooper University Hospital, Cooper Medical School of Rowan University, Camden, New Jersey, USA.
⁶⁶ Airlangga University, Surabaya, Jawa Timur, Indonesia.
⁶⁷ Neurointerventional Radiology, University of Massachusetts Medical School, Worcester, Massachusetts, USA.
⁶⁸ Interventional Neuroradiology, University Hospitals Geneva, Geneva, Switzerland.
⁶⁹ Interventional Neuroradiology, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil.
⁷⁰ Neuroscience and Behavioral Sciences, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil.
⁷¹ Interventional Neuroradiology, Beth Israel Lahey Health, Burlington, Massachusetts, USA.
⁷² Neurology, Beth Israel Lahey Health, Burlington, Massachusetts, USA.
⁷³ Radiology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA.
⁷⁴ Neurology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA.
⁷⁵ Memorial Neuroscience Institute, Pembroke Pines, Florida, USA.
⁷⁶ Neurosurgery, Iwate Prefectural Central Hospital, Morioka, Iwate, Japan.
⁷⁷ Neurosurgery, Kyoto Second Red Cross Hospital, Kyoto, Japan.
⁷⁸ Ajou University Hospital, Suwon, Gyeonggi-do, South Korea.
⁷⁹ Neurology, University of Ottawa, Ottawa, Ontario, Canada.
⁸⁰ Cerebrovascular Medicine, Saga-ken Medical Centre Koseikan, Saga, Japan.
⁸¹ Neurology, Neurosurgery, Radiology, University of South Alabama, Mobile, Alabama, USA.
⁸² Konkuk University, Gwangjin-gu, Seoul, South Korea.
⁸³ Interventional Neuroradiology, Royal London Hospital, Barts Health NHS Trust, London, UK.
⁸⁴ Neurology, Hospital Clinico Universitario de Valladolid, Valladolid, Castilla y León, Spain.
⁸⁵ Interventional Neuroradiology, Hospital Clínico Universitario, Universidad de Valladolid, Valladolid, Spain.
⁸⁶ INR, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain.
⁸⁷ Neurology, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain.
⁸⁸ Stroke Unit, Department of Medicine, Centro Hospitalar Universitário de São João, Porto, Portugal.
⁸⁹ Neuroradiology, Centro Hospitalar Universitário de São João, Porto, Portugal.
⁹⁰ Neurology, Christchurch Hospital, Christchurch, New Zealand.
⁹¹ Neurosurgery, Christchurch Hospital, Christchurch, New Zealand.
⁹² Interventional and Diagnostic Neuroradiology, University Hospital Basel, Basel, Switzerland.
⁹³ Neurosurgery, University of Southern California, Los Angeles, California, USA.
⁹⁴ Neurosurgery, Japanese Red Cross Kumamoto Hospital, Kumamoto, Kumamoto, Japan.
⁹⁵ Neurosurgery, Kohnan Hospital, Sendai, Miyagi, Japan.
⁹⁶ Radiology, Neurology, UT Southwestern, Dallas, Texas, USA.
⁹⁷ Endovascular Neurosurgery, Nara City Hospital, Nara, Nara, Japan.
⁹⁸ Neurology, Toyonaka Municipal Hospital, Toyonaka, Osaka, Japan.
⁹⁹ Neurosurgery and Stroke Center, Kagoshima City Hospital, Kagoshima, Kagoshima, Japan.
¹⁰⁰ Texas Tech University System, Lubbock, Texas, USA.
¹⁰¹ Neurosurgery, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
¹⁰² Neurosurgery, Jikei University School of Medicine, Minato-ku, Tokyo, Japan.
¹⁰³ Neurology, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia.
¹⁰⁴ Neurosurgery, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia.
¹⁰⁵ Neurosciences, Banner Desert Medical Center, Mesa, Arizona, USA.
¹⁰⁶ Neurology, Japanese Red Cross Matsue Hospital, Shimane, Japan.
¹⁰⁷ Neurology, Shiroyama Hospital, Habikino, Osaka, Japan.
¹⁰⁸ Cerebrovascular Medicine, Niigata City General Hospital, Niigata, Niigata, Japan.
¹⁰⁹ Neurology, Sugimura Hospital, Kumamoto, Japan.
¹¹⁰ Department of Neurosurgery, Kawasaki Medical School, Kurashiki, Japan.
¹¹¹ Neurology, Osaka Red Cross Hospital, Osaka, Japan.
¹¹² Neurosurgery, University of Tsukuba, Tsukuba, Ibaraki, Japan.
¹¹³ Neurology, Stroke Center and Neuroendovascular Therapy, Saiseikai Central Hospital, Minato-ku, Tokyo, Japan.
¹¹⁴ Neurology, Kinikyo Chuo Hospital, Sapporo, Hokkaido, Japan.
¹¹⁵ Cerebrovascular Medicine, NTT Medical Center Tokyo, Tokyo, Japan.
¹¹⁶ Neurosurgery, Yokohama Shintoshi Neurosurgical Hospital, Yokohama, Japan.
¹¹⁷ Neurosurgery, Osaka General Medical Center, Osaka, Japan.
¹¹⁸ Neurology, Neurosurgery, University of Miami School of Medicine, Miami, Florida, USA.
¹¹⁹ Neurology, Bon Secours Mercy Health System, Toledo, Ohio, USA.
¹²⁰ Neurology, Maoming City Hospital, Guandong, China.
¹²¹ Interventional Neuroradiology, Endovascular Neurosurgery, Miami Cardiac & Vascular Institute, Miami, Florida, USA.
¹²² Neurology, Hackensack Meridian Health, Edison, New Jersey, USA.
¹²³ Neurology, University of California Los Angeles, Los Angeles, California, USA.
¹²⁴ Interventional Neuroradiology, University of California Los Angeles, Los Angeles, California, USA.
¹²⁵ Neurology, Erlanger Medical Center, University of Tennessee, Chattanooga, Tennessee, USA.
¹²⁶ Neurology, Neurosurgery, Radiology, University of Texas Health San Antonio, San Antonio, Texas, USA.
¹²⁷ Neurology, Mianyang 404 Hospital, Mianyang, Sichuan, China.
¹²⁸ Radiology, Siriraj Hosital, Mahidol University, Bangkok, Thailand.
¹²⁹ Neurology, Neurosurgery, Radiology, SUNY Upstate Medical University, Syracuse, New York, USA.
¹³⁰ Neurosurgery, Royal North Shore Hospital, Sydney, New South Wales, Australia.
¹³¹ Neurosciences, The University of Texas Rio Grande Valley, Harlingen, Texas, USA.
¹³² Central Stroke Unit, Directorate of Neuroscience, Khoula Hospital, Ministry of Health, Muscat, Oman.
¹³³ Neurology, University of Michigan, Ann Arbor, Michigan, USA.
¹³⁴ Neurosurgery, University of South Florida, Tampa, Florida, USA.
¹³⁵ Neurology, Henry Ford Health System, Detroit, Michigan, USA.
¹³⁶ Stroke Unit, Metropolitan Hospital, Piraeus, Greece.
¹³⁷ Faculty of Medicine, National and Kapodistrian University of Athens, Athens, Greece.
¹³⁸ Neurology, Maine Medical Center, Portland, Maine, USA.
¹³⁹ Neuroradiology, Dartmouth Hitchcock Medical Center, Lebanon, New Hampshire, USA.
¹⁴⁰ Neurology, Hospital Universitario de Brasilia, Brasilia, Distrito Federal, Brazil.
¹⁴¹ Neurointerventional Neurosurgery, The Valley Hospital, Ridgewood, New Jersey, USA.
¹⁴² Neurosciences, Stroke Program, St Joseph's University Medical Center, Paterson, New Jersey, USA.
¹⁴³ Neurology, Christian Medical College and Hospital Ludhiana, Ludhiana, Punjab, India.
¹⁴⁴ Vascular Neurology Unit, Clínica Alemana, Universidad del Desarrollo, Santiago, Chile.
¹⁴⁵ Neurology, Osaka University Graduate School of Medicine, Osaka, Japan.
¹⁴⁶ Neurology, Tokushima University Hospital, Tokushima, Japan.
¹⁴⁷ Neurology, Universidade Federal de Sao Paulo, Sao Paulo, Sao Paulo, Brazil.
¹⁴⁸ Istanbul Aydin University, Istanbul, İstanbul, Turkey.
¹⁴⁹ Neurology, Bayhealth Medical Center, Dover, Delaware, USA.
¹⁵⁰ Neurology, Saiseikai Fukuoka General Hospital, Fukuoka, Japan.
¹⁵¹ Division of Stroke, Department of Internal Medicine, Osaka Rosai Hospital, Sakai, Osaka, Japan.
¹⁵² Neurology Division, Department of Medicine, King Saud University, Riyadh, Riyadh Province, Saudi Arabia.
¹⁵³ Neurology, Mount Sinai Health System, New York, New York, USA.
¹⁵⁴ Neurology, Clinical Neurosciences and Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada.
¹⁵⁵ Neurology, Affiliated Hangzhou First People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
¹⁵⁶ Neurology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China.
¹⁵⁷ Neurology, Yijishan Hospital of Wannan Medical College, Wuhu, Anhui, China.
¹⁵⁸ The University of Toledo, Toledo, Ohio, USA.
¹⁵⁹ Neuroscience, WellStar Health System, Marietta, Georgia, USA.
¹⁶⁰ Neuroradiologie Interventionelle, Centre Hospitalier de l'Université de Montréal, Montreal, Quebec, Canada.
¹⁶¹ Neurology, Marcus Stroke & Neuroscience Center, Grady Memorial Hospital, Emory University School of Medicine, Atlanta, GA, USA raul.g.nogueira@emory.edu.

^# Contributed equally.

PMID: 33771936
PMCID: PMC8006491
DOI: 10.1136/svn-2020-000695

Observational Study

Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic

Thanh N Nguyen et al. Stroke Vasc Neurol. 2021 Dec.

. 2021 Dec;6(4):542-552.

doi: 10.1136/svn-2020-000695. Epub 2021 Mar 26.

Authors

Affiliations

¹ Neurology, Radiology, Boston Medical Center, Boston, Massachusetts, USA.
² Neurology, Marcus Stroke & Neuroscience Center, Grady Memorial Hospital, Emory University School of Medicine, Atlanta, GA, USA.
³ Radiology, Radiation Oncology, Boston University School of Medicine, Boston, Massachusetts, USA.
⁴ Neurology, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁵ Neurosurgery, National Hospital Organization Osaka National Hospital, Osaka, Japan.
⁶ Neurology, Alexandria University, Alexandria, Egypt.
⁷ Radiology, Boston Medical Center, Boston, Massachusetts, USA.
⁸ Department of Neurology, Xinqiao Hospital, Chongqing, China.
⁹ Neurosurgery, University of Cape Town, Rondebosch, Western Cape, South Africa.
¹⁰ Neurosurgery, Interventional Neuroradiology, Clinica La Sagrada Familia, Buenos Aires, Argentina.
¹¹ Neuroradiologie, Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France.
¹² Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France.
¹³ Interventional Neuroradiology, Fondation Ophtalmologique Adolphe de Rothschild, Paris, Île-de-France, France.
¹⁴ Neurology, Hospital Geral de Fortaleza, Fortaleza, Brazil.
¹⁵ Interventional Neuroradiology, Hospital Geral de Fortaleza, Fortaleza, Brazil.
¹⁶ Neuroradiology, Nottingham University Hospitals NHS Trust, Nottingham, UK.
¹⁷ Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
¹⁸ Interventional Neurovascular Unit, University Hospital Careggi, Firenze, Toscana, Italy.
¹⁹ Neuroradiology, University Hospital Centre Zagreb, Zagreb, Croatia.
²⁰ Interventional Neuroradiology, Hopital Bicetre, Le Kremlin-Bicetre, France.
²¹ Stroke and Interventional Neuroradiology, Lahore General Hospital, Lahore, Pakistan.
²² Neurological Institute, Cleveland Clinic Abu Dhabi, Abu Dhabi, UAE.
²³ Department of Radiology, Beaumont Hospital, Dublin, Ireland.
²⁴ Neurology, Stroke Unit, Hospital-Estadual Central, Vitoria, Brazil.
²⁵ Neuroradiology, Instituto de Neurocirugia Dr Asengo, Santiago, Chile.
²⁶ Interventional Neuroradiology, Institut National de Neurologie, Tunis, Tunisia.
²⁷ Neurology, Boston Medical Center, Boston, Massachusetts, USA.
²⁸ Neurosurgery, Boston Medical Center, Boston, MA, USA.
²⁹ Stroke Center, Hue Central Hospital, Hue, Thua Thien Hue, Vietnam.
³⁰ Radiology, University of California San Francisco, San Francisco, California, USA.
³¹ Interventional Neuroradiology, University of California San Francisco, San Francisco, California, USA.
³² Neuroradiologie Diagnostique et Interventionnelle, Hôpital Guillaume & René Laennec, CHU Nantes, Nantes, France.
³³ Neurological Surgery, University of Washington School of Medicine, Seattle, Washington, USA.
³⁴ Neurology, University of Washington School of Medicine, Seattle, Washington, USA.
³⁵ Radiology, Swedish Medical Center, Englewood, Colorado, USA.
³⁶ Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, Pennsylvania, USA.
³⁷ Neurology, Neurosurgery, Westchester Medical Center Health Network, Valhalla, New York, USA.
³⁸ Stroke and Neurointervention Unit, Eskisehir OsmangaziUniversity, Eskisehir, Turkey.
³⁹ Radiology, Neurology, Neurosurgery, University of Maryland School of Medicine, Baltimore, Maryland, USA.
⁴⁰ Interventional Neurology, MAX Superspecialty Hospital, Saket, New Delhi, India.
⁴¹ Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA.
⁴² Neurosurgery, Centre Hospitalier Universitaire de Québec-Université Laval, Quebec, Quebec, Canada.
⁴³ Neurology, St Louis University School of Medicine, St Louis, Missouri, USA.
⁴⁴ Neurological Surgery, Rush University Medical Center, Chicago, IL, USA.
⁴⁵ Neurology, Research Institute of Neurointervention, University Hospital Salzburg /Paracelsus Medical University, Salzburg, Austria.
⁴⁶ Neurosurgery, Medical Imaging, Surgery, University of Toronto, Toronto, Ontario, Canada.
⁴⁷ Neurology, NH Mazumdar Shah Medical Center, Bangalore, India.
⁴⁸ Neurology, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan.
⁴⁹ Stroke and Neurovascular Surgery, IMS Tokyo-Katsushika General Hospital, Tokyo, Japan.
⁵⁰ Gachon University, Seongnam, Korea (the Republic of).
⁵¹ Stroke Unit, Hospital Municipal Sao Jose, Joinville, Santa Catarina, Brazil.
⁵² Interventional Neuroradiology, Lau Medical Center, Beirut, Lebanon.
⁵³ Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa, USA.
⁵⁴ Neurosurgery, Royal Adelaide Hospital, Adelaide, South Australia, Australia.
⁵⁵ Stroke and Cerebrovascular Medicine, Kyorin University, Mitaka, Tokyo, Japan.
⁵⁶ Neurology, Yokohama Brain and Spine Center, Yokohama, Japan.
⁵⁷ Neurosurgery, Dalhousie University, Halifax, Nova Scotia, Canada.
⁵⁸ Radiology, QEII Health Sciences Centre, Dalhousie University, Dalhousie, Nova Scotia, Canada.
⁵⁹ Interventional Neuroradiology, Rambam Health Care Campus, Haifa, Haifa, Israel.
⁶⁰ Centro Endovascular Neurologico Medica Uruguaya, Montevideo, Uruguay.
⁶¹ Neuroradiology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany.
⁶² Neurology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany.
⁶³ Neurosurgery, Interventional Radiology and Critical Care Medicine, King Fahad Hospital of the University, Imam Abdulrahman bin Faisal University, Alkhobar, Saudi Arabia.
⁶⁴ Neurology, University of Texas McGovern Medical School, Houston, Texas, USA.
⁶⁵ Neurology, Cooper University Hospital, Cooper Medical School of Rowan University, Camden, New Jersey, USA.
⁶⁶ Airlangga University, Surabaya, Jawa Timur, Indonesia.
⁶⁷ Neurointerventional Radiology, University of Massachusetts Medical School, Worcester, Massachusetts, USA.
⁶⁸ Interventional Neuroradiology, University Hospitals Geneva, Geneva, Switzerland.
⁶⁹ Interventional Neuroradiology, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil.
⁷⁰ Neuroscience and Behavioral Sciences, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil.
⁷¹ Interventional Neuroradiology, Beth Israel Lahey Health, Burlington, Massachusetts, USA.
⁷² Neurology, Beth Israel Lahey Health, Burlington, Massachusetts, USA.
⁷³ Radiology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA.
⁷⁴ Neurology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA.
⁷⁵ Memorial Neuroscience Institute, Pembroke Pines, Florida, USA.
⁷⁶ Neurosurgery, Iwate Prefectural Central Hospital, Morioka, Iwate, Japan.
⁷⁷ Neurosurgery, Kyoto Second Red Cross Hospital, Kyoto, Japan.
⁷⁸ Ajou University Hospital, Suwon, Gyeonggi-do, South Korea.
⁷⁹ Neurology, University of Ottawa, Ottawa, Ontario, Canada.
⁸⁰ Cerebrovascular Medicine, Saga-ken Medical Centre Koseikan, Saga, Japan.
⁸¹ Neurology, Neurosurgery, Radiology, University of South Alabama, Mobile, Alabama, USA.
⁸² Konkuk University, Gwangjin-gu, Seoul, South Korea.
⁸³ Interventional Neuroradiology, Royal London Hospital, Barts Health NHS Trust, London, UK.
⁸⁴ Neurology, Hospital Clinico Universitario de Valladolid, Valladolid, Castilla y León, Spain.
⁸⁵ Interventional Neuroradiology, Hospital Clínico Universitario, Universidad de Valladolid, Valladolid, Spain.
⁸⁶ INR, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain.
⁸⁷ Neurology, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain.
⁸⁸ Stroke Unit, Department of Medicine, Centro Hospitalar Universitário de São João, Porto, Portugal.
⁸⁹ Neuroradiology, Centro Hospitalar Universitário de São João, Porto, Portugal.
⁹⁰ Neurology, Christchurch Hospital, Christchurch, New Zealand.
⁹¹ Neurosurgery, Christchurch Hospital, Christchurch, New Zealand.
⁹² Interventional and Diagnostic Neuroradiology, University Hospital Basel, Basel, Switzerland.
⁹³ Neurosurgery, University of Southern California, Los Angeles, California, USA.
⁹⁴ Neurosurgery, Japanese Red Cross Kumamoto Hospital, Kumamoto, Kumamoto, Japan.
⁹⁵ Neurosurgery, Kohnan Hospital, Sendai, Miyagi, Japan.
⁹⁶ Radiology, Neurology, UT Southwestern, Dallas, Texas, USA.
⁹⁷ Endovascular Neurosurgery, Nara City Hospital, Nara, Nara, Japan.
⁹⁸ Neurology, Toyonaka Municipal Hospital, Toyonaka, Osaka, Japan.
⁹⁹ Neurosurgery and Stroke Center, Kagoshima City Hospital, Kagoshima, Kagoshima, Japan.
¹⁰⁰ Texas Tech University System, Lubbock, Texas, USA.
¹⁰¹ Neurosurgery, University of Saskatchewan, Saskatoon, Saskatchewan, Canada.
¹⁰² Neurosurgery, Jikei University School of Medicine, Minato-ku, Tokyo, Japan.
¹⁰³ Neurology, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia.
¹⁰⁴ Neurosurgery, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia.
¹⁰⁵ Neurosciences, Banner Desert Medical Center, Mesa, Arizona, USA.
¹⁰⁶ Neurology, Japanese Red Cross Matsue Hospital, Shimane, Japan.
¹⁰⁷ Neurology, Shiroyama Hospital, Habikino, Osaka, Japan.
¹⁰⁸ Cerebrovascular Medicine, Niigata City General Hospital, Niigata, Niigata, Japan.
¹⁰⁹ Neurology, Sugimura Hospital, Kumamoto, Japan.
¹¹⁰ Department of Neurosurgery, Kawasaki Medical School, Kurashiki, Japan.
¹¹¹ Neurology, Osaka Red Cross Hospital, Osaka, Japan.
¹¹² Neurosurgery, University of Tsukuba, Tsukuba, Ibaraki, Japan.
¹¹³ Neurology, Stroke Center and Neuroendovascular Therapy, Saiseikai Central Hospital, Minato-ku, Tokyo, Japan.
¹¹⁴ Neurology, Kinikyo Chuo Hospital, Sapporo, Hokkaido, Japan.
¹¹⁵ Cerebrovascular Medicine, NTT Medical Center Tokyo, Tokyo, Japan.
¹¹⁶ Neurosurgery, Yokohama Shintoshi Neurosurgical Hospital, Yokohama, Japan.
¹¹⁷ Neurosurgery, Osaka General Medical Center, Osaka, Japan.
¹¹⁸ Neurology, Neurosurgery, University of Miami School of Medicine, Miami, Florida, USA.
¹¹⁹ Neurology, Bon Secours Mercy Health System, Toledo, Ohio, USA.
¹²⁰ Neurology, Maoming City Hospital, Guandong, China.
¹²¹ Interventional Neuroradiology, Endovascular Neurosurgery, Miami Cardiac & Vascular Institute, Miami, Florida, USA.
¹²² Neurology, Hackensack Meridian Health, Edison, New Jersey, USA.
¹²³ Neurology, University of California Los Angeles, Los Angeles, California, USA.
¹²⁴ Interventional Neuroradiology, University of California Los Angeles, Los Angeles, California, USA.
¹²⁵ Neurology, Erlanger Medical Center, University of Tennessee, Chattanooga, Tennessee, USA.
¹²⁶ Neurology, Neurosurgery, Radiology, University of Texas Health San Antonio, San Antonio, Texas, USA.
¹²⁷ Neurology, Mianyang 404 Hospital, Mianyang, Sichuan, China.
¹²⁸ Radiology, Siriraj Hosital, Mahidol University, Bangkok, Thailand.
¹²⁹ Neurology, Neurosurgery, Radiology, SUNY Upstate Medical University, Syracuse, New York, USA.
¹³⁰ Neurosurgery, Royal North Shore Hospital, Sydney, New South Wales, Australia.
¹³¹ Neurosciences, The University of Texas Rio Grande Valley, Harlingen, Texas, USA.
¹³² Central Stroke Unit, Directorate of Neuroscience, Khoula Hospital, Ministry of Health, Muscat, Oman.
¹³³ Neurology, University of Michigan, Ann Arbor, Michigan, USA.
¹³⁴ Neurosurgery, University of South Florida, Tampa, Florida, USA.
¹³⁵ Neurology, Henry Ford Health System, Detroit, Michigan, USA.
¹³⁶ Stroke Unit, Metropolitan Hospital, Piraeus, Greece.
¹³⁷ Faculty of Medicine, National and Kapodistrian University of Athens, Athens, Greece.
¹³⁸ Neurology, Maine Medical Center, Portland, Maine, USA.
¹³⁹ Neuroradiology, Dartmouth Hitchcock Medical Center, Lebanon, New Hampshire, USA.
¹⁴⁰ Neurology, Hospital Universitario de Brasilia, Brasilia, Distrito Federal, Brazil.
¹⁴¹ Neurointerventional Neurosurgery, The Valley Hospital, Ridgewood, New Jersey, USA.
¹⁴² Neurosciences, Stroke Program, St Joseph's University Medical Center, Paterson, New Jersey, USA.
¹⁴³ Neurology, Christian Medical College and Hospital Ludhiana, Ludhiana, Punjab, India.
¹⁴⁴ Vascular Neurology Unit, Clínica Alemana, Universidad del Desarrollo, Santiago, Chile.
¹⁴⁵ Neurology, Osaka University Graduate School of Medicine, Osaka, Japan.
¹⁴⁶ Neurology, Tokushima University Hospital, Tokushima, Japan.
¹⁴⁷ Neurology, Universidade Federal de Sao Paulo, Sao Paulo, Sao Paulo, Brazil.
¹⁴⁸ Istanbul Aydin University, Istanbul, İstanbul, Turkey.
¹⁴⁹ Neurology, Bayhealth Medical Center, Dover, Delaware, USA.
¹⁵⁰ Neurology, Saiseikai Fukuoka General Hospital, Fukuoka, Japan.
¹⁵¹ Division of Stroke, Department of Internal Medicine, Osaka Rosai Hospital, Sakai, Osaka, Japan.
¹⁵² Neurology Division, Department of Medicine, King Saud University, Riyadh, Riyadh Province, Saudi Arabia.
¹⁵³ Neurology, Mount Sinai Health System, New York, New York, USA.
¹⁵⁴ Neurology, Clinical Neurosciences and Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada.
¹⁵⁵ Neurology, Affiliated Hangzhou First People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China.
¹⁵⁶ Neurology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China.
¹⁵⁷ Neurology, Yijishan Hospital of Wannan Medical College, Wuhu, Anhui, China.
¹⁵⁸ The University of Toledo, Toledo, Ohio, USA.
¹⁵⁹ Neuroscience, WellStar Health System, Marietta, Georgia, USA.
¹⁶⁰ Neuroradiologie Interventionelle, Centre Hospitalier de l'Université de Montréal, Montreal, Quebec, Canada.
¹⁶¹ Neurology, Marcus Stroke & Neuroscience Center, Grady Memorial Hospital, Emory University School of Medicine, Atlanta, GA, USA raul.g.nogueira@emory.edu.

^# Contributed equally.

PMID: 33771936
PMCID: PMC8006491
DOI: 10.1136/svn-2020-000695

Abstract

Background: During the COVID-19 pandemic, decreased volumes of stroke admissions and mechanical thrombectomy were reported. The study's objective was to examine whether subarachnoid haemorrhage (SAH) hospitalisations and ruptured aneurysm coiling interventions demonstrated similar declines.

Methods: We conducted a cross-sectional, retrospective, observational study across 6 continents, 37 countries and 140 comprehensive stroke centres. Patients with the diagnosis of SAH, aneurysmal SAH, ruptured aneurysm coiling interventions and COVID-19 were identified by prospective aneurysm databases or by International Classification of Diseases, 10th Revision, codes. The 3-month cumulative volume, monthly volumes for SAH hospitalisations and ruptured aneurysm coiling procedures were compared for the period before (1 year and immediately before) and during the pandemic, defined as 1 March-31 May 2020. The prior 1-year control period (1 March-31 May 2019) was obtained to account for seasonal variation.

Findings: There was a significant decline in SAH hospitalisations, with 2044 admissions in the 3 months immediately before and 1585 admissions during the pandemic, representing a relative decline of 22.5% (95% CI -24.3% to -20.7%, p<0.0001). Embolisation of ruptured aneurysms declined with 1170-1035 procedures, respectively, representing an 11.5% (95%CI -13.5% to -9.8%, p=0.002) relative drop. Subgroup analysis was noted for aneurysmal SAH hospitalisation decline from 834 to 626 hospitalisations, a 24.9% relative decline (95% CI -28.0% to -22.1%, p<0.0001). A relative increase in ruptured aneurysm coiling was noted in low coiling volume hospitals of 41.1% (95% CI 32.3% to 50.6%, p=0.008) despite a decrease in SAH admissions in this tertile.

Interpretation: There was a relative decrease in the volume of SAH hospitalisations, aneurysmal SAH hospitalisations and ruptured aneurysm embolisations during the COVID-19 pandemic. These findings in SAH are consistent with a decrease in other emergencies, such as stroke and myocardial infarction.

Keywords: aneurysm; coil; haemorrhage; infection; subarachnoid.

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Conflict of interest statement

Competing interests: TNN: PI CLEAR study (Medtronic). DCH: Stryker, Vesalio, Cerenovus consultant. AEH: consultant and speaker for Medtronic, Stryker, Microvention, Penumbra, Balt, Scientia, Genentech and GE Healthcare. PJ: Medtronic, Microvention, Balt, Cerenovus consultant. SO-G: Medtronic, Stryker consultant. DSL: Cerenovus, Genentech, Stryker, Medtronic consultant. TGJ: advisor/investor for Anaconda, Route92, FreeOx, and Blockade Medical; Medtronic grants, DAWN, AURORA PI (Stryker). WJM: consultant: Rebound Therapeutics, Viseon Imperative Care, Q’Apel, Stryker, Stream Biomedical, Spartan Micro; Investor: Cerebrotech, Endostream, Q’Apel, Viseon, Rebound, and Spartan Micro. RGN: Stryker; Cerenovus/Neuravi; Anaconda, Cerebrotech, Ceretrieve, Vesalio (Advisory Board); Imperative Care.

Figures

**Figure 1**
*Peak of 1235 COVID-19 hospitalisations in the second week of February, predominantly from one hospital in Wuhan, China. SAH, subarachnoid haemorrhage.

See this image and copyright information in PMC

References

1. Emanuel EJ, Persad G, Upshur R, et al. . Fair allocation of scarce medical resources in the time of Covid-19. N Engl J Med Overseas Ed 2020;382:2049–55. 10.1056/NEJMsb2005114 - DOI - PubMed
1. Nguyen TN, Jadhav AP, Dasenbrock HH, et al. . Subarachnoid hemorrhage guidance in the era of the COVID-19 pandemic - An opinion to mitigate exposure and conserve personal protective equipment. J Stroke Cerebrovasc Dis 2020;29:105010. 10.1016/j.jstrokecerebrovasdis.2020.105010 - DOI - PMC - PubMed
1. Nguyen TN, Abdalkader M, Jovin TG, et al. . Mechanical thrombectomy in the era of the COVID-19 pandemic: emergency preparedness for neuroscience teams: a guidance statement from the Society of vascular and Interventional Neurology. Stroke 2020;51:1896–901. 10.1161/STROKEAHA.120.030100 - DOI - PMC - PubMed
1. Nogueira RG, Qureshi M, Abdalkader M. Global impact of COVID-19 on stroke care and intravenous thrombolysis. American Academy of Neurology; April 17-22, 2021.
1. Alonso de Leciñana M, Castellanos M, Ayo-Martín Óscar, et al. . Stroke care during the COVID-19 outbreak in Spain: the experience of Spanish stroke units. Stroke Vasc Neurol 2020. 10.1136/svn-2020-000678. [Epub ahead of print: 04 Dec 2020]. - DOI - PMC - PubMed

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Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic

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Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic

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