Article Text

Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic
  1. Thanh N Nguyen1,
  2. Diogo C Haussen2,
  3. Muhammad M Qureshi3,
  4. Hiroshi Yamagami4,
  5. Toshiyuki Fujinaka5,
  6. Ossama Y Mansour6,
  7. Mohamad Abdalkader7,
  8. Michael Frankel2,
  9. Zhongming Qiu8,
  10. Allan Taylor9,
  11. Pedro Lylyk10,
  12. Omer F Eker11,
  13. Laura Mechtouff12,
  14. Michel Piotin13,
  15. Fabricio Oliveira Lima14,
  16. Francisco Mont'Alverne15,
  17. Wazim Izzath16,
  18. Nobuyuki Sakai17,
  19. Mahmoud Mohammaden2,
  20. Alhamza R Al-Bayati2,
  21. Leonardo Renieri18,
  22. Salvatore Mangiafico18,
  23. David Ozretic19,
  24. Vanessa Chalumeau20,
  25. Saima Ahmad21,
  26. Umair Rashid21,
  27. Syed Irteza Hussain22,
  28. Seby John22,
  29. Emma Griffin23,
  30. John Thornton23,
  31. Jose Antonio Fiorot24,
  32. Rodrigo Rivera25,
  33. Nadia Hammami26,
  34. Anna M Cervantes-Arslanian27,
  35. Hormuzdiyar H Dasenbrock28,
  36. Huynh Le Vu29,
  37. Viet Quy Nguyen29,
  38. Steven Hetts30,31,
  39. Romain Bourcier32,
  40. Romain Guile32,
  41. Melanie Walker33,
  42. Malveeka Sharma34,
  43. Don Frei35,
  44. Pascal Jabbour36,
  45. Nabeel Herial36,
  46. Fawaz Al-Mufti37,
  47. Atilla Ozcan Ozdemir38,
  48. Ozlem Aykac38,
  49. Dheeraj Gandhi39,
  50. Chandril Chugh40,
  51. Charles Matouk41,
  52. Pascale Lavoie42,
  53. Randall Edgell43,
  54. Andre Beer-Furlan44,
  55. Michael Chen44,
  56. Monika Killer-Oberpfalzer45,
  57. Vitor Mendes Pereira46,
  58. Patrick Nicholson46,
  59. Vikram Huded47,
  60. Nobuyuki Ohara48,
  61. Daisuke Watanabe49,
  62. Dong Hun Shin50,
  63. Pedro SC Magalhaes51,
  64. Raghid Kikano52,
  65. Santiago Ortega-Gutierrez53,
  66. Mudassir Farooqui53,
  67. Amal Abou-Hamden54,
  68. Tatsuo Amano55,
  69. Ryoo Yamamoto56,
  70. Adrienne Weeks57,
  71. Elena A Cora58,
  72. Rotem Sivan-Hoffmann59,
  73. Roberto Crosa60,
  74. Markus Möhlenbruch61,
  75. Simon Nagel62,
  76. Hosam Al-Jehani63,
  77. Sunil A Sheth64,
  78. Victor S Lopez Rivera64,
  79. James E Siegler65,
  80. Achmad Fidaus Sani66,
  81. Ajit S Puri67,
  82. Anna Luisa Kuhn67,
  83. Gianmarco Bernava68,
  84. Paolo Machi68,
  85. Daniel G Abud69,
  86. Octavio M Pontes-Neto70,
  87. Ajay K Wakhloo71,
  88. Barbara Voetsch72,
  89. Eytan Raz73,
  90. Shadi Yaghi74,
  91. Brijesh P Mehta75,
  92. Naoto Kimura76,
  93. Mamoru Murakami77,
  94. Jin Soo Lee78,
  95. Ji Man Hong78,
  96. Robert Fahed79,
  97. Gregory Walker79,
  98. Eiji Hagashi80,
  99. Steve M Cordina81,
  100. Hong Gee Roh82,
  101. Ken Wong83,
  102. Juan F Arenillas84,
  103. Mario Martinez-Galdamez85,
  104. Jordi Blasco86,
  105. Alejandro Rodriguez Vasquez87,
  106. Luisa Fonseca88,
  107. M Luis Silva89,
  108. Teddy Y Wu90,
  109. Simon John91,
  110. Alex Brehm92,
  111. Marios Psychogios92,
  112. William J Mack93,
  113. Matthew Tenser93,
  114. Tatemi Todaka94,
  115. Miki Fujimura95,
  116. Roberta Novakovic96,
  117. Jun Deguchi97,
  118. Yuri Sugiura98,
  119. Hiroshi Tokimura99,
  120. Rakesh Khatri100,
  121. Michael Kelly101,
  122. Lissa Peeling101,
  123. Yuichi Murayama102,
  124. Hugh Stephen Winters103,
  125. Johnny Wong104,
  126. Mohamed Teleb105,
  127. Jeremy Payne105,
  128. Hiroki Fukuda106,
  129. Kosuke Miyake107,
  130. Junsuke Shimbo108,
  131. Yusuke Sugimura109,
  132. Masaaki Uno110,
  133. Yohei Takenobu111,
  134. Yuji Matsumaru112,
  135. Satoshi Yamada113,
  136. Ryuhei Kono114,
  137. Takuya Kanamaru115,
  138. Masafumi Morimoto116,
  139. Junichi Iida117,
  140. Vasu Saini118,
  141. Dileep Yavagal118,
  142. Saif Bushnaq119,
  143. Wenguo Huang120,
  144. Italo Linfante121,
  145. Jawad Kirmani122,
  146. David S Liebeskind123,
  147. Viktor Szeder124,
  148. Ruchir Shah125,
  149. Thomas G Devlin125,
  150. Lee Birnbaum126,
  151. Jun Luo127,
  152. Anchalee Churojana128,
  153. Hesham E Masoud129,
  154. Carlos Ynigo Lopez129,
  155. Brendan Steinfort130,
  156. Alice Ma130,
  157. Ameer E Hassan131,
  158. Amal Al Hashmi132,
  159. Mollie McDermott133,
  160. Maxim Mokin134,
  161. Alex Chebl135,
  162. Odysseas Kargiotis136,
  163. Georgios Tsivgoulis137,
  164. Jane G Morris138,
  165. Clifford J Eskey139,
  166. Jesse Thon65,
  167. Leticia Rebello140,
  168. Dorothea Altschul141,
  169. Oriana Cornett142,
  170. Varsha Singh142,
  171. Jeyaraj Pandian143,
  172. Anirudh Kulkarni143,
  173. Pablo M Lavados144,
  174. Veronica V Olavarria144,
  175. Kenichi Todo145,
  176. Yuki Yamamoto146,
  177. Gisele Sampaio Silva147,
  178. Serdar Geyik148,
  179. Jasmine Johann35,
  180. Sumeet Multani149,
  181. Artem Kaliaev7,
  182. Kazutaka Sonoda150,
  183. Hiroyuki Hashimoto151,
  184. Adel Alhazzani152,
  185. David Y Chung27,
  186. Stephan A Mayer37,
  187. Johanna T Fifi153,
  188. Michael D Hill154,
  189. Hao Zhang155,
  190. Zhengzhou Yuan156,
  191. Xianjin Shang157,
  192. Alicia C Castonguay158,
  193. Rishi Gupta159,
  194. Tudor G Jovin65,
  195. Jean Raymond160,
  196. Osama O Zaidat119,
  197. Raul G Nogueira2,
  198. SVIN COVID-19 Registry, the Middle East North Africa Stroke and Interventional Neurotherapies Organization (MENA-SINO)
  199. Japanese Society of Vascular and Interventional Neurology Society (JVIN)
  1. 1Neurology, Radiology, Boston Medical Center, Boston, Massachusetts, USA
  2. 2Neurology, Marcus Stroke & Neuroscience Center, Grady Memorial Hospital, Emory University School of Medicine, Atlanta, GA, USA
  3. 3Radiology, Radiation Oncology, Boston University School of Medicine, Boston, Massachusetts, USA
  4. 4Neurology, National Hospital Organization Osaka National Hospital, Osaka, Japan
  5. 5Neurosurgery, National Hospital Organization Osaka National Hospital, Osaka, Japan
  6. 6Neurology, Alexandria University, Alexandria, Egypt
  7. 7Radiology, Boston Medical Center, Boston, Massachusetts, USA
  8. 8Department of Neurology, Xinqiao Hospital, Chongqing, China
  9. 9Neurosurgery, University of Cape Town, Rondebosch, Western Cape, South Africa
  10. 10Neurosurgery, Interventional Neuroradiology, Clinica La Sagrada Familia, Buenos Aires, Argentina
  11. 11Neuroradiologie, Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France
  12. 12Neurologie Vasculaire, Hospices Civils de Lyon, Lyon, Auvergne-Rhône-Alpes, France
  13. 13Interventional Neuroradiology, Fondation Ophtalmologique Adolphe de Rothschild, Paris, Île-de-France, France
  14. 14Neurology, Hospital Geral de Fortaleza, Fortaleza, Brazil
  15. 15Interventional Neuroradiology, Hospital Geral de Fortaleza, Fortaleza, Brazil
  16. 16Neuroradiology, Nottingham University Hospitals NHS Trust, Nottingham, UK
  17. 17Department of Neurosurgery, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan
  18. 18Interventional Neurovascular Unit, University Hospital Careggi, Firenze, Toscana, Italy
  19. 19Neuroradiology, University Hospital Centre Zagreb, Zagreb, Croatia
  20. 20Interventional Neuroradiology, Hopital Bicetre, Le Kremlin-Bicetre, France
  21. 21Stroke and Interventional Neuroradiology, Lahore General Hospital, Lahore, Pakistan
  22. 22Neurological Institute, Cleveland Clinic Abu Dhabi, Abu Dhabi, UAE
  23. 23Department of Radiology, Beaumont Hospital, Dublin, Ireland
  24. 24Neurology, Stroke Unit, Hospital-Estadual Central, Vitoria, Brazil
  25. 25Neuroradiology, Instituto de Neurocirugia Dr Asengo, Santiago, Chile
  26. 26Interventional Neuroradiology, Institut National de Neurologie, Tunis, Tunisia
  27. 27Neurology, Boston Medical Center, Boston, Massachusetts, USA
  28. 28Neurosurgery, Boston Medical Center, Boston, MA, USA
  29. 29Stroke Center, Hue Central Hospital, Hue, Thua Thien Hue, Vietnam
  30. 30Radiology, University of California San Francisco, San Francisco, California, USA
  31. 31Interventional Neuroradiology, University of California San Francisco, San Francisco, California, USA
  32. 32Neuroradiologie Diagnostique et Interventionnelle, Hôpital Guillaume & René Laennec, CHU Nantes, Nantes, France
  33. 33Neurological Surgery, University of Washington School of Medicine, Seattle, Washington, USA
  34. 34Neurology, University of Washington School of Medicine, Seattle, Washington, USA
  35. 35Radiology, Swedish Medical Center, Englewood, Colorado, USA
  36. 36Neurosurgery, Thomas Jefferson University Hospital, Philadelphia, Pennsylvania, USA
  37. 37Neurology, Neurosurgery, Westchester Medical Center Health Network, Valhalla, New York, USA
  38. 38Stroke and Neurointervention Unit, Eskisehir OsmangaziUniversity, Eskisehir, Turkey
  39. 39Radiology, Neurology, Neurosurgery, University of Maryland School of Medicine, Baltimore, Maryland, USA
  40. 40Interventional Neurology, MAX Superspecialty Hospital, Saket, New Delhi, India
  41. 41Neurosurgery, Yale School of Medicine, New Haven, Connecticut, USA
  42. 42Neurosurgery, Centre Hospitalier Universitaire de Québec-Université Laval, Quebec, Quebec, Canada
  43. 43Neurology, St Louis University School of Medicine, St Louis, Missouri, USA
  44. 44Neurological Surgery, Rush University Medical Center, Chicago, IL, USA
  45. 45Neurology, Research Institute of Neurointervention, University Hospital Salzburg /Paracelsus Medical University, Salzburg, Austria
  46. 46Neurosurgery, Medical Imaging, Surgery, University of Toronto, Toronto, Ontario, Canada
  47. 47Neurology, NH Mazumdar Shah Medical Center, Bangalore, India
  48. 48Neurology, Kobe City Medical Center General Hospital, Kobe, Hyogo, Japan
  49. 49Stroke and Neurovascular Surgery, IMS Tokyo-Katsushika General Hospital, Tokyo, Japan
  50. 50Gachon University, Seongnam, Korea (the Republic of)
  51. 51Stroke Unit, Hospital Municipal Sao Jose, Joinville, Santa Catarina, Brazil
  52. 52Interventional Neuroradiology, Lau Medical Center, Beirut, Lebanon
  53. 53Neurology, University of Iowa Hospitals and Clinics, Iowa City, Iowa, USA
  54. 54Neurosurgery, Royal Adelaide Hospital, Adelaide, South Australia, Australia
  55. 55Stroke and Cerebrovascular Medicine, Kyorin University, Mitaka, Tokyo, Japan
  56. 56Neurology, Yokohama Brain and Spine Center, Yokohama, Japan
  57. 57Neurosurgery, Dalhousie University, Halifax, Nova Scotia, Canada
  58. 58Radiology, QEII Health Sciences Centre, Dalhousie University, Dalhousie, Nova Scotia, Canada
  59. 59Interventional Neuroradiology, Rambam Health Care Campus, Haifa, Haifa, Israel
  60. 60Centro Endovascular Neurologico Medica Uruguaya, Montevideo, Uruguay
  61. 61Neuroradiology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany
  62. 62Neurology, Heidelberg University Hospital, Heidelberg, Baden-Württemberg, Germany
  63. 63Neurosurgery, Interventional Radiology and Critical Care Medicine, King Fahad Hospital of the University, Imam Abdulrahman bin Faisal University, Alkhobar, Saudi Arabia
  64. 64Neurology, University of Texas McGovern Medical School, Houston, Texas, USA
  65. 65Neurology, Cooper University Hospital, Cooper Medical School of Rowan University, Camden, New Jersey, USA
  66. 66Airlangga University, Surabaya, Jawa Timur, Indonesia
  67. 67Neurointerventional Radiology, University of Massachusetts Medical School, Worcester, Massachusetts, USA
  68. 68Interventional Neuroradiology, University Hospitals Geneva, Geneva, Switzerland
  69. 69Interventional Neuroradiology, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil
  70. 70Neuroscience and Behavioral Sciences, Ribeirão Preto Medical School, University of São Paulo, São Paulo, Brazil
  71. 71Interventional Neuroradiology, Beth Israel Lahey Health, Burlington, Massachusetts, USA
  72. 72Neurology, Beth Israel Lahey Health, Burlington, Massachusetts, USA
  73. 73Radiology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA
  74. 74Neurology, NYU Langone Health, NYU Grossman School of Medicine, New York, New York, USA
  75. 75Memorial Neuroscience Institute, Pembroke Pines, Florida, USA
  76. 76Neurosurgery, Iwate Prefectural Central Hospital, Morioka, Iwate, Japan
  77. 77Neurosurgery, Kyoto Second Red Cross Hospital, Kyoto, Japan
  78. 78Ajou University Hospital, Suwon, Gyeonggi-do, South Korea
  79. 79Neurology, University of Ottawa, Ottawa, Ontario, Canada
  80. 80Cerebrovascular Medicine, Saga-ken Medical Centre Koseikan, Saga, Japan
  81. 81Neurology, Neurosurgery, Radiology, University of South Alabama, Mobile, Alabama, USA
  82. 82Konkuk University, Gwangjin-gu, Seoul, South Korea
  83. 83Interventional Neuroradiology, Royal London Hospital, Barts Health NHS Trust, London, UK
  84. 84Neurology, Hospital Clinico Universitario de Valladolid, Valladolid, Castilla y León, Spain
  85. 85Interventional Neuroradiology, Hospital Clínico Universitario, Universidad de Valladolid, Valladolid, Spain
  86. 86INR, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain
  87. 87Neurology, Hospital Clinic de Barcelona, Barcelona, Catalunya, Spain
  88. 88Stroke Unit, Department of Medicine, Centro Hospitalar Universitário de São João, Porto, Portugal
  89. 89Neuroradiology, Centro Hospitalar Universitário de São João, Porto, Portugal
  90. 90Neurology, Christchurch Hospital, Christchurch, New Zealand
  91. 91Neurosurgery, Christchurch Hospital, Christchurch, New Zealand
  92. 92Interventional and Diagnostic Neuroradiology, University Hospital Basel, Basel, Switzerland
  93. 93Neurosurgery, University of Southern California, Los Angeles, California, USA
  94. 94Neurosurgery, Japanese Red Cross Kumamoto Hospital, Kumamoto, Kumamoto, Japan
  95. 95Neurosurgery, Kohnan Hospital, Sendai, Miyagi, Japan
  96. 96Radiology, Neurology, UT Southwestern, Dallas, Texas, USA
  97. 97Endovascular Neurosurgery, Nara City Hospital, Nara, Nara, Japan
  98. 98Neurology, Toyonaka Municipal Hospital, Toyonaka, Osaka, Japan
  99. 99Neurosurgery and Stroke Center, Kagoshima City Hospital, Kagoshima, Kagoshima, Japan
  100. 100Texas Tech University System, Lubbock, Texas, USA
  101. 101Neurosurgery, University of Saskatchewan, Saskatoon, Saskatchewan, Canada
  102. 102Neurosurgery, Jikei University School of Medicine, Minato-ku, Tokyo, Japan
  103. 103Neurology, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia
  104. 104Neurosurgery, Royal Prince Alfred Hospital, Camperdown, New South Wales, Australia
  105. 105Neurosciences, Banner Desert Medical Center, Mesa, Arizona, USA
  106. 106Neurology, Japanese Red Cross Matsue Hospital, Shimane, Japan
  107. 107Neurology, Shiroyama Hospital, Habikino, Osaka, Japan
  108. 108Cerebrovascular Medicine, Niigata City General Hospital, Niigata, Niigata, Japan
  109. 109Neurology, Sugimura Hospital, Kumamoto, Japan
  110. 110Department of Neurosurgery, Kawasaki Medical School, Kurashiki, Japan
  111. 111Neurology, Osaka Red Cross Hospital, Osaka, Japan
  112. 112Neurosurgery, University of Tsukuba, Tsukuba, Ibaraki, Japan
  113. 113Neurology, Stroke Center and Neuroendovascular Therapy, Saiseikai Central Hospital, Minato-ku, Tokyo, Japan
  114. 114Neurology, Kinikyo Chuo Hospital, Sapporo, Hokkaido, Japan
  115. 115Cerebrovascular Medicine, NTT Medical Center Tokyo, Tokyo, Japan
  116. 116Neurosurgery, Yokohama Shintoshi Neurosurgical Hospital, Yokohama, Japan
  117. 117Neurosurgery, Osaka General Medical Center, Osaka, Japan
  118. 118Neurology, Neurosurgery, University of Miami School of Medicine, Miami, Florida, USA
  119. 119Neurology, Bon Secours Mercy Health System, Toledo, Ohio, USA
  120. 120Neurology, Maoming City Hospital, Guandong, China
  121. 121Interventional Neuroradiology, Endovascular Neurosurgery, Miami Cardiac & Vascular Institute, Miami, Florida, USA
  122. 122Neurology, Hackensack Meridian Health, Edison, New Jersey, USA
  123. 123Neurology, University of California Los Angeles, Los Angeles, California, USA
  124. 124Interventional Neuroradiology, University of California Los Angeles, Los Angeles, California, USA
  125. 125Neurology, Erlanger Medical Center, University of Tennessee, Chattanooga, Tennessee, USA
  126. 126Neurology, Neurosurgery, Radiology, University of Texas Health San Antonio, San Antonio, Texas, USA
  127. 127Neurology, Mianyang 404 Hospital, Mianyang, Sichuan, China
  128. 128Radiology, Siriraj Hosital, Mahidol University, Bangkok, Thailand
  129. 129Neurology, Neurosurgery, Radiology, SUNY Upstate Medical University, Syracuse, New York, USA
  130. 130Neurosurgery, Royal North Shore Hospital, Sydney, New South Wales, Australia
  131. 131Neurosciences, The University of Texas Rio Grande Valley, Harlingen, Texas, USA
  132. 132Central Stroke Unit, Directorate of Neuroscience, Khoula Hospital, Ministry of Health, Muscat, Oman
  133. 133Neurology, University of Michigan, Ann Arbor, Michigan, USA
  134. 134Neurosurgery, University of South Florida, Tampa, Florida, USA
  135. 135Neurology, Henry Ford Health System, Detroit, Michigan, USA
  136. 136Stroke Unit, Metropolitan Hospital, Piraeus, Greece
  137. 137Faculty of Medicine, National and Kapodistrian University of Athens, Athens, Greece
  138. 138Neurology, Maine Medical Center, Portland, Maine, USA
  139. 139Neuroradiology, Dartmouth Hitchcock Medical Center, Lebanon, New Hampshire, USA
  140. 140Neurology, Hospital Universitario de Brasilia, Brasilia, Distrito Federal, Brazil
  141. 141Neurointerventional Neurosurgery, The Valley Hospital, Ridgewood, New Jersey, USA
  142. 142Neurosciences, Stroke Program, St Joseph’s University Medical Center, Paterson, New Jersey, USA
  143. 143Neurology, Christian Medical College and Hospital Ludhiana, Ludhiana, Punjab, India
  144. 144Vascular Neurology Unit, Clínica Alemana, Universidad del Desarrollo, Santiago, Chile
  145. 145Neurology, Osaka University Graduate School of Medicine, Osaka, Japan
  146. 146Neurology, Tokushima University Hospital, Tokushima, Japan
  147. 147Neurology, Universidade Federal de Sao Paulo, Sao Paulo, Sao Paulo, Brazil
  148. 148Istanbul Aydin University, Istanbul, İstanbul, Turkey
  149. 149Neurology, Bayhealth Medical Center, Dover, Delaware, USA
  150. 150Neurology, Saiseikai Fukuoka General Hospital, Fukuoka, Japan
  151. 151Division of Stroke, Department of Internal Medicine, Osaka Rosai Hospital, Sakai, Osaka, Japan
  152. 152Neurology Division, Department of Medicine, King Saud University, Riyadh, Riyadh Province, Saudi Arabia
  153. 153Neurology, Mount Sinai Health System, New York, New York, USA
  154. 154Neurology, Clinical Neurosciences and Hotchkiss Brain Institute, University of Calgary, Calgary, Alberta, Canada
  155. 155Neurology, Affiliated Hangzhou First People's Hospital, Zhejiang University School of Medicine, Hangzhou, Zhejiang, China
  156. 156Neurology, The Affiliated Hospital of Southwest Medical University, Luzhou, Sichuan, China
  157. 157Neurology, Yijishan Hospital of Wannan Medical College, Wuhu, Anhui, China
  158. 158The University of Toledo, Toledo, Ohio, USA
  159. 159Neuroscience, WellStar Health System, Marietta, Georgia, USA
  160. 160Neuroradiologie Interventionelle, Centre Hospitalier de l'Université de Montréal, Montreal, Quebec, Canada
  1. Correspondence to Dr Raul G Nogueira; raul.g.nogueira{at}emory.edu

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.

  • aneurysm
  • coil
  • haemorrhage
  • infection
  • subarachnoid
http://creativecommons.org/licenses/by-nc/4.0/

This is an open access article distributed in accordance with the Creative Commons Attribution Non Commercial (CC BY-NC 4.0) license, which permits others to distribute, remix, adapt, build upon this work non-commercially, and license their derivative works on different terms, provided the original work is properly cited, appropriate credit is given, any changes made indicated, and the use is non-commercial. See: http://creativecommons.org/licenses/by-nc/4.0/.

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Background

The COVID-19 pandemic led to the rationing of healthcare resources worldwide to accommodate the care of critically ill patients with SARS-CoV-2 infection.1 Changes in prehospital emergency medical service, emergency room care, acute stroke and subarachnoid haemorrhage (SAH) protocols2 3 were reported to conserve resources and to mitigate infection risk to patients and their providers. Decreases in ischaemic stroke admission, rates of intravenous thrombolysis (IVT)4–6 and mechanical thrombectomy (MT) volume7 were reported in several regions in Europe,8 9 Germany,10 China,11 Brazil12 and the USA,13 14 with steeper declines in stroke hospitalisations seen in areas with higher COVID-19 hospitalisation volume.15

However, there is a paucity of information on the impact of the COVID-19 pandemic on SAH admissions. Early regional or single-centre reports from Paris16 and Toronto17 suggest a decrease in aneurysmal SAH volumes, whereas no changes were seen in Berlin.18 We evaluated the impact of COVID-19 on the volumes of SAH admissions and embolisation treatments for patients with ruptured intracranial aneurysms during the height of the first 3 months of the pandemic, defined from 1 March to 31 May 2020.

Study objectives and hypothesis

Our primary hypothesis was that there would be a reduction in SAH hospitalisations and endovascular coil embolisation procedures for ruptured aneurysms during the pandemic, compared with the immediate 3 months prior to the pandemic. Our secondary hypothesis was that there would be a reduction in these volumes compared with a similar calendar period in 2019. The third hypothesis was that the reduction in SAH volume would occur in most centres, including those with low or non-existent COVID-19 hospitalisation burden, but would be more significant in centres with high COVID-19 hospitalisation burden. The fourth hypothesis was that high procedural coiling volume centres would be less impacted by procedural volume changes than low procedural volume centres.

Methods

Study design

This was a cross-sectional, observational, multicentre, retrospective study of consecutive patients hospitalised with SAH, aneurysmal SAH, non-traumatic SAH and ruptured intracranial aneurysm embolisations.

Setting and participants

Of 175 invited sites, 140 comprehensive stroke centres submitted data from 37 countries across six continents with 5571 patients with SAH and 3473 ruptured aneurysm embolisations across the three different study periods. Monthly and weekly volume of SAH, ruptured aneurysm embolisations and COVID-19 admission volume data were collected over three periods of time: 1 March–31 May 2020 (pandemic months), 1 November 2019–29 February 2020 (immediately preceding the pandemic months) and 1 March–31 May 2019 (equivalent period 1 year prior to the pandemic). The period of recruitment was conducted between 26 May and 30 July 2020. The data were collected on Excel (version 16.45) documents.

Data were collected from collaborators of the Society of Vascular and Interventional Neurology, the Middle East North Africa Stoke and Interventional Neurotherapies Organisation, the Japanese Interventional Neurology Society and several academic partners. The following countries were represented (number of centres): USA (45), Japan (30), China (6), Brazil (6), Canada (6), France (4), Australia (3), Korea (3), India (3), Chile (2), Spain (2), Switzerland (2), England (2), Saudi Arabia (2), Turkey (2), Austria (1), Argentina (1), Egypt (1), Germany (1), Vietnam (1), Croatia (1), Greece (1), Indonesia (1), Ireland (1), Israel (1), Italy (1), Lebanon (1), New Zealand (1), Oman (1), Pakistan (1), Portugal (1) Qatar (1), South Africa (1), Thailand (1), Tunisia (1), United Arab Emirates (1) and Uruguay (1).

Study variables and outcome measures

SAH data were obtained by a prospectively maintained aneurysm or stroke databases at each comprehensive stroke centre or by International Classification of Diseases, 10th Revision (ICD-10) codes (primary, secondary or tertiary discharge codes) with verification by a physician or coordinator. The following ICD-10 codes were used: I60 (non-traumatic SAH), I60.0 (non-traumatic SAH from carotid siphon and bifurcation), I60.1 (non-traumatic SAH from middle cerebral artery), I60.2 (non-traumatic SAH from anterior communicating artery), I60.3 (non-traumatic SAH from posterior communicating artery), I60.4 (non-traumatic SAH from basilar artery), I60.5 (non-traumatic SAH from vertebral artery, I60.6 (non-traumatic SAH from other intracranial arteries), I60.7 (non-traumatic SAH from intracranial artery, unspecified) I60.8 (other non-traumatic SAH) and I60.9 (non-traumatic SAH unspecified).

Subgroup analysis of confirmed aneurysmal SAH hospitalisations and non-traumatic SAH were performed. Aneurysmal SAH was defined as SAH related to a ruptured intracranial aneurysm. Non-traumatic SAH was defined as SAH unrelated to traumatic causes but could include SAH secondary to aneurysmal, arteriovenous malformation (AVM), perimesencephalic or other causes. The volume of embolisations of ruptured intracranial aneurysms was also retrieved.

COVID-19 hospitalisation was defined as a patient admitted with COVID-19 diagnosis, inclusive of non-neurological diagnosis. Monthly and weekly volumes of COVID-19 hospitalisation were collected from 1 March to 31 May 2020.

Low, intermediate and high procedural volume centres were categorised according to monthly coiling of ruptured aneurysm volume data received of the 4 months immediately preceding the pandemic (1 November 2019–29 February 2020, inclusive) and divided into tertiles: low volume, <1.25; intermediate volume, >1.25–<3.0; and high volume, >3 coiling cases per month. COVID-19 hospitalisation volumes were based on mean monthly volume data received and were divided into tertiles: low volume, <10.6; intermediate volume, >10.6–<103.6; and high volume, >103.6 hospitalisations per month.

Bias

A second control period (1 March–31 May 2019) was included to account for seasonal variation. To reduce the risk of bias, centres with incomplete data were excluded from the subgroup analysis in which the data were missing.

Statistical analysis

The monthly volumes for the ruptured aneurysm coil embolisation procedure and SAH admissions were compared for the period before (1 year and immediately before) and during the COVID-19 pandemic. The normality of the data was tested with the Shapiro-Wilk test. The data were determined to be non-normal and were therefore presented as median (IQR). The non-parametric Wilcoxon signed-rank test was applied to compare differences in monthly volume between two time periods. The analyses were repeated in the setting of low, intermediate and high COVID-19 and procedural volume hospitals.

We further looked at the percentage change in the number of procedures and SAH admissions, aneurysmal SAH admissions, and non-traumatic SAH admissions before and during the COVID-19 pandemic. For this analysis, we restricted the immediately before group to 3 months before the pandemic (1 December 2019–29 February 2020) to keep it consistent with the COVID-19 group. The 95% CIs for percentage change were calculated using the Wilson procedure without correction for continuity. The differences in the number of procedures and admissions across the two periods were assessed for significance using the Poisson means test. The relative percentage decrease in volume between low-volume, intermediate-volume and high-volume hospitals was tested using the z‐test of proportion.

We performed a supplementary analysis comparing monthly volumes and percentage change in the number of ruptured aneurysm coiling procedures and SAH hospitalisations across different world regions. All data were analysed using SAS V.9.4, and the significance level was set at a p value of <0.05.

This study is reported in accordance with the Strengthening the Reporting of Observational Studies in Epidemiology guidelines.19

Findings

A total of 1088, 2044 and 1585 SAH hospitalisations (overall n=4717) and 719, 1170 and 1035 coiling procedures for ruptured aneurysms (overall n=2924) were included across the 3-month prior year periods, 3 months immediately prepandemic and 3 months pandemic, respectively. These were distributed across 140 comprehensive stroke centres, 37 nations and 6 continents. The Shapiro-Wilk test revealed that the normality of the data was non-normal.

Subarachnoid hemorrhage hospitalisation volumes

In the primary analysis, 118 centres submitted data on SAH volume with a total of 2044 admissions in the 3 months immediately before and 1585 admissions during the 3 months of the pandemic, representing a relative volume decline of 22.5% (95% CI −24.3% to −20.7%, p<0.0001). Monthly SAH admission volumes also demonstrated a relative decline before and during the pandemic months (median, 4.5 (IQR 2.5–7.1) vs 3.3 (IQR1.3–6.3); p<0.0001) (table 1 and figure 1).

Table 1

SAH hospitalisation volumes immediately before and during the COVID-19 pandemic

Figure 1

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

In the secondary analysis, 75 centres contributed data with SAH monthly volumes 1 year prior (table 2). There were 1088 before, compared with 900 SAH admissions during the pandemic, representing a 17.3% relative decline (95% CI, −19.6 to −15.2, p<0.0001). The median monthly SAH admission volume declined from a median of 3.0 [IQR, 2.0–6.3] in the corresponding period of the prior year to 2.7 [IQR, 1.3–5.7, p=0.001] over the first 3 months of the pandemic.

Table 2

SAH volumes 1 year before and during the COVID-19 pandemic

In subgroup analysis, 56 centres confirmed aneurysmal SAH admissions data in the 3 months immediately before and during the pandemic. There was a relative decline from 834 to 626 hospitalisations, representing a 24.9% relative decline (95% CI −28.0% to −22.1%, p<0.0001). Additionally, 37 centres confirmed aneurysmal SAH admissions data in the 1-year prior control period, also noted for a relative decline from 435 to 370 hospitalisations, representing a 14.9% relative decline (95% CI −18.6 to −11.9, p=0.022) (table 3).

Table 3

Aneurysmal SAH, non-traumatic SAH hospitalisations before and during the pandemic

Non-traumatic SAH admissions had parallel relative declines both in the immediately before (−24.6%, 95% CI −26.9% to −22.5%, p<0.0001, n=85 centres) and 1-year before periods (−15.6%, 95% CI −18.4% to −13.1%, p=0.002, n=53 centres) (table 3).

Declines in SAH hospitalisation volumes were significant in Asia, with a relative decrease of 24.7% (95% CI −28.0% to −21.7%, p<0.0001, n=47 centres); North America, with a relative decrease of 21.0% (95% CI −24.0% to −18.3%, p<0.0001, n=46 centres); Europe, with a relative decrease of 29.0% (95% CI −35.3% to −23.5%, p=0.001, n=11 centres); South America, with a relative decrease of 21.5% (95% CI −27.4% to −16.6%, p=0.012, n=8 centres). In contrast, no significant change was noted in Oceania or Africa. (online supplemental table 1). Country-specific relative changes in SAH hospitalisation volumes are represented in online supplemental table 3 and online supplemental figure 1).

Supplemental material

SAH aneurysm embolisation volumes

In the primary analysis, 125 centres submitted data on ruptured aneurysm embolisation volumes with a total of 1170 procedures in the 3 months immediately before and 1035 procedures performed during the 3 months of the pandemic, representing a relative drop of 11.5% (95% CI −13.5% to −9.8%, p=0.002). Median monthly embolisation volumes demonstrated a relative decline compared with the same periods immediately preceding (median, 1.8 (IQR 1–4) vs 1.7 (IQR 0.67–3.3); p=0.0004) (table 4 and figure 1).

Table 4

SAH coil embolisation volumes immediately before and during the COVID-19 pandemic

In the secondary analysis, 83 centres contributed data for ruptured aneurysm coiled volumes during the pandemic and 1 year previously. Ruptured aneurysm embolisations also declined numerically between the calendar year, 719 vs 652 procedures, with a 9.3% (95% CI −11.7% to −7.4%, p=0.07) relative drop in volumes (table 2). No significant change was noted in the median monthly volume (p=0.197).

During the pandemic, ruptured aneurysm coiling volume was decreased in Asia with a 20.5% relative decline (95% CI −24.9% to −16.6%, p=0.003, n=52 centres), decreased in Europe with a 15.3% relative decline (95% CI −20.4% to −11.3%, p=0.06, n=14 centres) and increased in Oceania by 77.8% (95% CI 54.8 to 91.0, p=0.06, n=4 centres), whereas no significant change in volume was noted in North America, South America nor Africa (online supplemental table 2). Country-specific relative changes in ruptured aneurysm coiling volumes are represented in online supplemental table 3 and online supplemental figure 2.

COVID-19 hospitalisation volume, SAH hospitalisation and ruptured aneurysm embolisation volumes in relation to the pandemic

Figure 1 depicts the weekly number of SAH hospitalisations, ruptured aneurysm coiling and COVID-19 hospitalisation volumes. Across the tertiles of COVID-19 hospitalisation volume, high-volume COVID-19 centres (−29.8%, 95% CI −33.2% to −26.6%) were significantly more vulnerable to declines in SAH hospitalisation volumes than low-volume COVID-19 centres (−15.1%, 95% CI −18.7% to −12.0%; p<0.0001) (table 1).

Similarly, there was a gradient for greater decrease in ruptured aneurysm embolisation in high-volume COVID-19 centres (−22.2%, 95% CI −27.0% to −18.0%) compared with intermediate-volume (−10.0%, 95% CI −13.8% to −7.2%, p<0.0001) and low-volume (−1.5%, 95% CI −3.7% to −0.6%, p<0.001) COVID-19 centres (table 4).

Ruptured aneurysm procedural volumes, SAH hospitalisation and ruptured aneurysm embolisation volumes in relation to the pandemic

There were declines in SAH hospitalisation volume across the three tertiles of high (−22.8%, 95% CI −25.5% to −20.3%, p<0.0001), intermediate (−21.4%, 95% CI −25.3% to −18.0%, p=0.0002) and low (−20.8% 95% CI −25.2% to −17.0%, p=0.002) SAH procedural volume centres, with no differences in decline seen between the three tertiles (table 1).

Similarly, ruptured aneurysm embolisation volume declines were noted in high (−18.2%, 95% CI −20.9% to −15.8%, p<0.0001) procedural volume centres. However, in hospitals with low tertile procedural volumes, there was an increase noted in the coiling of the ruptured aneurysm during the pandemic of 41% (95% CI 32.3% to 50.6%, p=0.008) (table 4).

Discussion

We noted a decrease in the volume of SAH hospitalisations, aneurysmal SAH hospitalisations and embolisation of ruptured aneurysms during the first 3 months of the COVID-19 pandemic compared with the immediate prior months. Compared with the corresponding period in the prior year, there was a significant reduction in SAH hospitalisation volume, but no change was noted in the number of embolisation procedures for ruptured aneurysms. To our knowledge, this is the first report of a multicentre decrease in volumes for SAH hospitalisations, aneurysmal SAH hospitalisations and embolisation procedures for ruptured intracranial aneurysm during the COVID-19 pandemic. Our findings are similar to reported decreases in SAH city-wide in Paris during a 2-week period of the pandemic16 and decreases in a Toronto hospital,17 whereas Berlin and Joinville, South Brazil, reported no decreases in SAH during the COVID-19 pandemic.12 18

As expected, hospitals with higher tertiles of COVID-19 hospitalisation burden were more vulnerable to the decline in SAH admissions and ruptured aneurysm coiling volume. However, hospitals with lower COVID-19 hospitalisation burden also demonstrated decreases in SAH admissions, suggesting that access to hospital care was likely not a principal factor to explain the decrease.

High and intermediate procedural volume centres were more affected by declines in SAH hospitalisations and ruptured aneurysm embolisation than low-volume SAH coiling centres during the pandemic. In contrast, hospitals with low SAH coiling volumes at baseline demonstrated an increase in the coiling of ruptured aneurysms during the pandemic despite a significant decrease in total SAH admissions within this tertile of hospitals. An increase in ruptured aneurysm embolisations was observed in another recent multicentre study during the COVID-19 pandemic.20 This suggests a shift towards treating more patients with ruptured aneurysms with endovascular techniques during the pandemic, possibly to mitigate risks of perioperative infection to the patient and/or provider.

These findings of decreases in SAH volumes, including embolisation of ruptured aneurysms, are similar to reports of decreases in stroke admissions, intravenous thrombolysis, MT and acute ST-elevation myocardial infarction (STEMI) activations during the COVID-19 pandemic.10 13 21 As postulated with reasons for the decline in stroke admissions in the stroke literature,8 patients with milder presentations of aneurysmal SAH may be afraid to present to a hospital due to fear of contracting SARS-CoV-2 infection.

This analysis’s strength is the aggregate volume of data worldwide across diverse geography, allowing a high volume or sample size. We used two control periods for comparison; the immediately preceding 3 months and the same 3 months a year ago, to account for potential seasonal variations that may occur in the presentation of SAH.22

Study limitations

This study’s limitations are that while our cohort of centres inform an international, multicentre experience, it is not comprehensive without source data from national databases to account for regional differences in health systems of care. The diagnosis of SAH was obtained using ICD-10 codes in some centres. We cannot exclude the possibility of traumatic SAH. To differentiate from this possibility, we performed a subgroup analysis of confirmed aneurysmal SAH and non-traumatic SAH admissions and found similar relative declines in both control periods. Most centres contributing to these data have systems in place to track SAH admissions and coiling volumes; hence, the relative changes in volume from this analysis are likely robust. Details on patient SAH presentation grade, clinical outcomes and clipping volume were not collected as they were outside the scope of the study.

Our study definition of the beginning of the pandemic relates to the WHO designation on 11 March 2020. However, regions affected by the pandemic earlier, such as China, met the nadir of their SAH volumes prior to starting our defined pandemic period. As endovascular coiling remains unavailable in many low-income and lower-income to middle-income countries, specific geographical regions were not well represented (ie, Central Africa) in our study. Another shortcoming in selection bias is that several countries in which endovascular coiling is available were not represented in this study (ie, Eastern Europe, South America, Central America and Asia).

Interpretation

In conclusion, there was a relative decrease in the volume of SAH hospitalisations, aneurysmal SAH hospitalisations and ruptured aneurysm embolisation treatments during the first 3 months studied of the COVID-19 pandemic. There were steeper relative declines in SAH hospitalisations and SAH coiling volume in hospitals with higher COVID-19 volume. Among low-volume coiling SAH hospitals, there was a shift towards an increase in ruptured aneurysm coiling. These findings can inform regional neuroscience centres’ preparedness2 23 24 in the face of a potential second wave or resurgence of COVID-19.

Acknowledgments

The authors thank Judith Clark, RN, Boston Medical Center; Matt Metzinger, MBA, CPHQ; Kamini Patel, RN, MSN, MBA, CPHQ, Jefferson; Janis Ginnane, RN, Emory University Hospital.

References

Supplementary material

  • Supplementary Data

    This web only file has been produced by the BMJ Publishing Group from an electronic file supplied by the author(s) and has not been edited for content.

Footnotes

  • Twitter @NguyenThanhMD, @DiogoHaussen, @Ossama_Mansour, @AbdalkaderMD, @eneri_neuro, @MahmoudNeuro, @AlAlBayati1, @SaimaAh46545828, @neurofox, @DrLe2287, @VietquyNguyen, @bourcierromain1, @Mali27043317, @donfreimd, @PascalJabbourMD, @NabeelHerial, @almuftifawaz, @dgandhimd, @MatoukCharles, @dr_mchen, @VitorMendesPer1, @paddynicholson, @Neurorradio, @raghidkikano, @CerebrovascLab, @AANeurosurgeon, @Operatingnheels, @eacora, @NagelSimon, @HosamJehani, @SunilAShethMD, @JimSiegler, @AjitSPuri1, @GianmarcoBerna5, @neuroabud, @opontesnetoMD, @eytanraz, @ShadiYaghi2, @NeuroINX, @SteveCordina, @ArenillasJF, @DoctorGaldamez, @jordiblascoa, @Teddyyhwu, @MPeyT1, @Robin_Novakovic, @michaelebkelly, @stephen_winters, @StrokeVAN, @VSainiMD, @dyavagal, @italolinfante, @dliebesk, @drviktorszeder, @HMasoud_, @brendan_dr, @alicenomalice, @AmeerEHassan, @MokinMax, @AlexChebl, @OKargiotis, @DrAltschul, @anirudhvk, @pablolavados, @volavarria, @GiseleSampaioS, @artemka__crh, @AdelALHAZZANI, @chungmdphd, @stephanamayer, @johannatfifi, @mihill68, @TudorGJovin, @oozaidat

  • TNN and RGN contributed equally.

  • Contributors TNN and RGN conceived the project. They wrote the first draft of the paper with subsequent input from all coauthors. All coauthors played a major role in data acquisition and revision of the manuscript. MMQ was the lead statistician for this study and performed the analysis. MA prepared the global maps in the supplement.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial or not-for-profit sectors.

  • 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.

  • Patient consent for publication Not required.

  • Ethics approval The institutional review boards (IRBs) from the coordinating sites determined that because the investigators did not have access to protected health information nor any private identifiable information, the study did not meet the definition of human subject research and therefore no informed consent or IRB oversight was required.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data availability statement All data relevant to the study are included in the article or uploaded as supplementary information. Anonymised data are available upon reasonable request from the corresponding author.

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