Literature DB >> 33771936

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

Thanh N Nguyen1, Raul G Nogueira2, Diogo C Haussen3, Muhammad M Qureshi4, Hiroshi Yamagami5, Toshiyuki Fujinaka6, Ossama Y Mansour7, Mohamad Abdalkader8, Michael Frankel3, Zhongming Qiu9, Allan Taylor10, Pedro Lylyk11, Omer F Eker12, Laura Mechtouff13, Michel Piotin14, Fabricio Oliveira Lima15, Francisco Mont'Alverne16, Wazim Izzath17, Nobuyuki Sakai18, Mahmoud Mohammaden3, Alhamza R Al-Bayati3, Leonardo Renieri19, Salvatore Mangiafico19, David Ozretic20, Vanessa Chalumeau21, Saima Ahmad22, Umair Rashid22, Syed Irteza Hussain23, Seby John23, Emma Griffin24, John Thornton24, Jose Antonio Fiorot25, Rodrigo Rivera26, Nadia Hammami27, Anna M Cervantes-Arslanian28, Hormuzdiyar H Dasenbrock29, Huynh Le Vu30, Viet Quy Nguyen30, Steven Hetts31,32, Romain Bourcier33, Romain Guile33, Melanie Walker34, Malveeka Sharma35, Don Frei36, Pascal Jabbour37, Nabeel Herial37, Fawaz Al-Mufti38, Atilla Ozcan Ozdemir39, Ozlem Aykac39, Dheeraj Gandhi40, Chandril Chugh41, Charles Matouk42, Pascale Lavoie43, Randall Edgell44, Andre Beer-Furlan45, Michael Chen45, Monika Killer-Oberpfalzer46, Vitor Mendes Pereira47, Patrick Nicholson47, Vikram Huded48, Nobuyuki Ohara49, Daisuke Watanabe50, Dong Hun Shin51, Pedro Sc Magalhaes52, Raghid Kikano53, Santiago Ortega-Gutierrez54, Mudassir Farooqui54, Amal Abou-Hamden55, Tatsuo Amano56, Ryoo Yamamoto57, Adrienne Weeks58, Elena A Cora59, Rotem Sivan-Hoffmann60, Roberto Crosa61, Markus Möhlenbruch62, Simon Nagel63, Hosam Al-Jehani64, Sunil A Sheth65, Victor S Lopez Rivera65, James E Siegler66, Achmad Fidaus Sani67, Ajit S Puri68, Anna Luisa Kuhn68, Gianmarco Bernava69, Paolo Machi69, Daniel G Abud70, Octavio M Pontes-Neto71, Ajay K Wakhloo72, Barbara Voetsch73, Eytan Raz74, Shadi Yaghi75, Brijesh P Mehta76, Naoto Kimura77, Mamoru Murakami78, Jin Soo Lee79, Ji Man Hong79, Robert Fahed80, Gregory Walker80, Eiji Hagashi81, Steve M Cordina82, Hong Gee Roh83, Ken Wong84, Juan F Arenillas85, Mario Martinez-Galdamez86, Jordi Blasco87, Alejandro Rodriguez Vasquez88, Luisa Fonseca89, M Luis Silva90, Teddy Y Wu91, Simon John92, Alex Brehm93, Marios Psychogios93, William J Mack94, Matthew Tenser94, Tatemi Todaka95, Miki Fujimura96, Roberta Novakovic97, Jun Deguchi98, Yuri Sugiura99, Hiroshi Tokimura100, Rakesh Khatri101, Michael Kelly102, Lissa Peeling102, Yuichi Murayama103, Hugh Stephen Winters104, Johnny Wong105, Mohamed Teleb106, Jeremy Payne106, Hiroki Fukuda107, Kosuke Miyake108, Junsuke Shimbo109, Yusuke Sugimura110, Masaaki Uno111, Yohei Takenobu112, Yuji Matsumaru113, Satoshi Yamada114, Ryuhei Kono115, Takuya Kanamaru116, Masafumi Morimoto117, Junichi Iida118, Vasu Saini119, Dileep Yavagal119, Saif Bushnaq120, Wenguo Huang121, Italo Linfante122, Jawad Kirmani123, David S Liebeskind124, Viktor Szeder125, Ruchir Shah126, Thomas G Devlin126, Lee Birnbaum127, Jun Luo128, Anchalee Churojana129, Hesham E Masoud130, Carlos Ynigo Lopez130, Brendan Steinfort131, Alice Ma131, Ameer E Hassan132, Amal Al Hashmi133, Mollie McDermott134, Maxim Mokin135, Alex Chebl136, Odysseas Kargiotis137, Georgios Tsivgoulis138, Jane G Morris139, Clifford J Eskey140, Jesse Thon66, Leticia Rebello141, Dorothea Altschul142, Oriana Cornett143, Varsha Singh143, Jeyaraj Pandian144, Anirudh Kulkarni144, Pablo M Lavados145, Veronica V Olavarria145, Kenichi Todo146, Yuki Yamamoto147, Gisele Sampaio Silva148, Serdar Geyik149, Jasmine Johann36, Sumeet Multani150, Artem Kaliaev8, Kazutaka Sonoda151, Hiroyuki Hashimoto152, Adel Alhazzani153, David Y Chung28, Stephan A Mayer38, Johanna T Fifi154, Michael D Hill155, Hao Zhang156, Zhengzhou Yuan157, Xianjin Shang158, Alicia C Castonguay159, Rishi Gupta160, Tudor G Jovin66, Jean Raymond161, Osama O Zaidat120.   

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. © Author(s) (or their employer(s)) 2021. Re-use permitted under CC BY-NC. No commercial re-use. See rights and permissions. Published by BMJ.

Entities:  

Keywords:  aneurysm; coil; haemorrhage; infection; subarachnoid

Mesh:

Year:  2021        PMID: 33771936      PMCID: PMC8006491          DOI: 10.1136/svn-2020-000695

Source DB:  PubMed          Journal:  Stroke Vasc Neurol        ISSN: 2059-8696


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

Overall volumeMonthly volume
Nn1n2Relative (%) changeP valueNImmediatelybeforen=2838DuringCOVID-19n=1645Difference* (95% CI)P value
% (95% CI)Median (IQR)
Overall11820441585−22.5 (−24.3 to −20.7)<0.00011244.5 (2.5–7.1)3.3 (1.3–6.3)−0.88 (−1.1 to −0.58)<0.0001
Hospital COVID-19 volume†
 Low32432367−15.1 (−18.7 to −12.0)0.014333.5 (2.5–6.5)3.3 (1.7–6.0)−0.83 (−1.9 to 0.50)0.076
 Int32589458−22.2 (−25.8 to −19.1)<0.0001344.9 (3.5–6.8)3.7 (1.7–6.0)−0.83 (−1.9 to −0.17)0.001
 High33731513−29.8 (−33.2 to −26.6)<0.0001366.0 (3.0–8.4)4.2 (2.2–7.2)−1.0 (−2.0 to −0.67)<0.0001
Hospital SAH coil embolisation volume‡
 Low42370293−20.8 (−25.2 to −17.0)0.002452.5 (1.3–3.8)2.0 (1.0–3.3)−0.25 (−0.75 to 0.08)0.141
 Int35490385−21.4 (−25.3 to −18.0)0.0002364.4 (2.9–5.6)3.0 (1.5–4.7)−1.0 (−1.5 to −0.17)0.007
 High351014783−22.8 (−25.5 to −20.3)<0.0001367.3 (5.9–11.6)6.7 (4.0–9.3)−2.0 (−3.1 to −0.75)<0.0001

n1 is based on 3 months before the pandemic (December 2019–February 2020). Immediately before is based on 4 months before the pandemic (November 2019–February 2020). n2 and during COVID-19 are based on March 2020–May 2020.

P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).

*Difference denotes the median difference between the two time periods.

†P value: low versus Int=0.004, low versus high=<0.0001, Int versus high=0.002.

‡P value: low versus Int=0.831, low versus high=0.429, Int versus high=0.541.

Int, intermediate; N, number of hospitals; n, number of admissions; SAH, subarachnoid haemorrhage.

Figure 1

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

SAH hospitalisation volumes immediately before and during the COVID-19 pandemic n1 is based on 3 months before the pandemic (December 2019–February 2020). Immediately before is based on 4 months before the pandemic (November 2019–February 2020). n2 and during COVID-19 are based on March 2020–May 2020. P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis). *Difference denotes the median difference between the two time periods. †P value: low versus Int=0.004, low versus high=<0.0001, Int versus high=0.002. ‡P value: low versus Int=0.831, low versus high=0.429, Int versus high=0.541. Int, intermediate; N, number of hospitals; n, number of admissions; SAH, subarachnoid haemorrhage. *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

Overall volumeMonthly volume
Nn1n2Relative (%) changeP valueN1 year beforeDuringCOVID-19Difference* (95% CI)P value
% (95% CI)Median (IQR)
SAH751088900−17.3 (−19.6 to −15.2)<0.0001753.0 (2.0–6.3)2.7 (1.3–5.7)−0.33 (−1.0 to 0.0)0.001
Coil embolisation†83719652−9.3 (−11.7 to −7.4)0.071851.7 (0.67–3.7)1.3 (0.67–2.7)0.0 (−0.33 to 0.0)0.197

n1 and 1 year before are based on 3-month data 1 year before the pandemic (March 2019–May 2019). n2 and during COVID-19 are based on data from March 2020 to May 2020.

P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).

*Difference denotes the median difference between the two time periods.

†85 centres contributed 728 and 655 patients to 1 year before and during the COVID-19 period in the monthly volume analysis.

n, number of admissions/procedures; N, number of hospitals; SAH, subarachnoid haemorrhage.

SAH volumes 1 year before and during the COVID-19 pandemic n1 and 1 year before are based on 3-month data 1 year before the pandemic (March 2019–May 2019). n2 and during COVID-19 are based on data from March 2020 to May 2020. P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis). *Difference denotes the median difference between the two time periods. †85 centres contributed 728 and 655 patients to 1 year before and during the COVID-19 period in the monthly volume analysis. n, number of admissions/procedures; N, number of hospitals; SAH, subarachnoid haemorrhage. 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

Immediately before and during the pandemic1 year before and during the pandemic
Nn1n2Relative change % (95% CI)P valueNn1n2Relative change % (95% CI)P value
Aneurysmal SAH56834626−24.9 (−28.0 to −22.1)<0.000137435370−14.9 (−18.6 to −11.9)0.022
Non-traumatic SAH*8514511094−24.6 (−26.9 to −22.5)<0.000153744628−15.6 (−18.4 to −13.1)0.002

n1 immediately before the pandemic is based on 3-month data from December 2019 to February 2020. n1 1 year before is based on 3-month data from March 2019 to May 2019. n2 is based on 3-month control data during the COVID-19 from March 2020 to May 2020 for both analyses.

P value is from the Poisson means test.

*Non-traumatic SAH include aneurysms and perimesencephalic SAH.

n, number of admissions; N, number of hospitals; SAH, subarachnoid haemorrhage.

Aneurysmal SAH, non-traumatic SAH hospitalisations before and during the pandemic n1 immediately before the pandemic is based on 3-month data from December 2019 to February 2020. n1 1 year before is based on 3-month data from March 2019 to May 2019. n2 is based on 3-month control data during the COVID-19 from March 2020 to May 2020 for both analyses. P value is from the Poisson means test. *Non-traumatic SAH include aneurysms and perimesencephalic SAH. n, number of admissions; N, number of hospitals; SAH, subarachnoid haemorrhage. 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).

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

Overall volumeMonthly volume
Nn1n2Relative (%) changeP valueNImmediately beforen=1670During COVID-19n=1075Difference* (95% CI)P value
% (95% CI)Median (IQR)
Overall12511701035−11.5 (−13.5 to −9.8)0.0021331.8 (1.0–4.0)1.7 (0.67–3.3)−0.25 (−0.58 to −0.08)0.0004
Hospital COVID-19 volume†
 Low39270266−1.5 (−3.7 to −0.58)0.764401.5 (0.88–2.5)1.0 (0.50–2.8)−0.29 (−0.67 to 0.08)0.294
 Int33319287−10.0 (−13.8 to −7.2)0.151352.5 (1.0–3.8)2.0 (1.0–3.0)−0.25 (−0.75 to 0.0)0.041
 High31329256−22.2 (−27.0 to −18.0)0.002342.0 (1.3–5.0)2.0 (1.0–4.0)−0.63 (−1.2 to 0.0)0.007
Hospital SAH Coil embolisation volume‡
 Low46107151 41.1 (32.3 to 50.6)0.008490.75 (0.25–1.0)0.67 (0.33–1.7)0.0 (0.0 to 0.33)0.044
 Int37217192−11.5 (−16.5 to −7.9)0.178392.0 (1.8–2.5)1.3 (0.67–2.7)−0.75 (−1.1 to −0.08)0.015
 High42846692−18.2 (−20.9 to −15.8)<0.0001455.3 (4.0–8.8)4.7 (2.7–6.3)−1.8 (−2.3 to −0.67)<0.0001

n1 is based on 3 months before the pandemic (December 2019–February 2020). Immediately before is based on 4 months before the pandemic (November 2019–February 2020). n2 and during COVID-19 are based on March 2020–May 2020.

P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis).

*Difference denotes the median difference between the two time periods.

†P value: low versus Int≤0.0001, low versus high≤0.0001, Int versus high≤0.0001.

‡P value: low versus Int=n/a; low versus high=n/a; Int versus high=0.019.

Int, intermediate; N, number of hospitals; n, number of procedures; n/a, not applicable; SAH, subarachnoid haemorrhage.

SAH coil embolisation volumes immediately before and during the COVID-19 pandemic n1 is based on 3 months before the pandemic (December 2019–February 2020). Immediately before is based on 4 months before the pandemic (November 2019–February 2020). n2 and during COVID-19 are based on March 2020–May 2020. P value is from Poisson means test (overall volume analysis) and Wilcoxon signed-rank test (monthly volume analysis). *Difference denotes the median difference between the two time periods. †P value: low versus Int≤0.0001, low versus high≤0.0001, Int versus high≤0.0001. ‡P value: low versus Int=n/a; low versus high=n/a; Int versus high=0.019. Int, intermediate; N, number of hospitals; n, number of procedures; n/a, not applicable; SAH, subarachnoid haemorrhage. 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.
  11 in total

1.  Non-ischemic neurovascular emergencies at a supra-regional medical center during the SARS-CoV2-pandemia.

Authors:  Konstantinos Lintas; Stefan Rohde; Gisa Ellrichmann; Boris El-Hamalawi; Robert Sarge; Thorsten Strohmann; Oliver Müller
Journal:  Clin Neurol Neurosurg       Date:  2022-07-19       Impact factor: 1.885

Review 2.  Therapeutic Trends of Cerebrovascular Disease during the COVID-19 Pandemic and Future Perspectives.

Authors:  James E Siegler; Mohamad Abdalkader; Patrik Michel; Thanh N Nguyen
Journal:  J Stroke       Date:  2022-05-31       Impact factor: 8.632

3.  Global Impact of the COVID-19 Pandemic on Cerebral Venous Thrombosis and Mortality.

Authors:  Thanh N Nguyen; Muhammad M Qureshi; Piers Klein; Hiroshi Yamagami; Mohamad Abdalkader; Robert Mikulik; Anvitha Sathya; Ossama Yassin Mansour; Anna Czlonkowska; Hannah Lo; Thalia S Field; Andreas Charidimou; Soma Banerjee; Shadi Yaghi; James E Siegler; Petra Sedova; Joseph Kwan; Diana Aguiar de Sousa; Jelle Demeestere; Violiza Inoa; Setareh Salehi Omran; Liqun Zhang; Patrik Michel; Davide Strambo; João Pedro Marto; Raul G Nogueira; Espen Saxhaug Kristoffersen; Georgios Tsivgoulis; Virginia Pujol Lereis; Alice Ma; Christian Enzinger; Thomas Gattringer; Aminur Rahman; Thomas Bonnet; Noémie Ligot; Sylvie De Raedt; Robin Lemmens; Peter Vanacker; Fenne Vandervorst; Adriana Bastos Conforto; Raquel C T Hidalgo; Daissy Liliana Mora Cuervo; Luciana de Oliveira Neves; Isabelle Lameirinhas da Silva; Rodrigo Targa Martíns; Letícia C Rebello; Igor Bessa Santiago; Teodora Sakelarova; Rosen Kalpachki; Filip Alexiev; Elena Adela Cora; Michael E Kelly; Lissa Peeling; Aleksandra Pikula; Hui-Sheng Chen; Yimin Chen; Shuiquan Yang; Marina Roje Bedekovic; Martin Čabal; Dusan Tenora; Petr Fibrich; Pavel Dušek; Helena Hlaváčová; Emanuela Hrabanovska; Lubomír Jurák; Jana Kadlčíková; Igor Karpowicz; Lukáš Klečka; Martin Kovář; Jiří Neumann; Hana Paloušková; Martin Reiser; Vladimir Rohan; Libor Šimůnek; Ondreij Skoda; Miroslav Škorňa; Martin Šrámek; Nicolas Drenck; Khalid Sobh; Emilie Lesaine; Candice Sabben; Peggy Reiner; Francois Rouanet; Daniel Strbian; Stefan Boskamp; Joshua Mbroh; Simon Nagel; Michael Rosenkranz; Sven Poli; Götz Thomalla; Theodoros Karapanayiotides; Ioanna Koutroulou; Odysseas Kargiotis; Lina Palaiodimou; José Dominguo Barrientos Guerra; Vikram Huded; Shashank Nagendra; Chintan Prajapati; P N Sylaja; Achmad Firdaus Sani; Abdoreza Ghoreishi; Mehdi Farhoudi; Elyar Sadeghi Hokmabadi; Mazyar Hashemilar; Sergiu Ionut Sabetay; Fadi Rahal; Maurizio Acampa; Alessandro Adami; Marco Longoni; Raffaele Ornello; Leonardo Renieri; Michele Romoli; Simona Sacco; Andrea Salmaggi; Davide Sangalli; Andrea Zini; Kenichiro Sakai; Hiroki Fukuda; Kyohei Fujita; Hirotoshi Imamura; Miyake Kosuke; Manabu Sakaguchi; Kazutaka Sonoda; Yuji Matsumaru; Nobuyuki Ohara; Seigo Shindo; Yohei Takenobu; Takeshi Yoshimoto; Kazunori Toyoda; Takeshi Uwatoko; Nobuyuki Sakai; Nobuaki Yamamoto; Ryoo Yamamoto; Yukako Yazawa; Yuri Sugiura; Jang-Hyun Baek; Si Baek Lee; Kwon-Duk Seo; Sung-Il Sohn; Jin Soo Lee; Anita Ante Arsovska; Chan Yong Chieh; Wan Asyraf Wan Zaidi; Wan Nur Nafisah Wan Yahya; Fernando Gongora-Rivera; Manuel Martinez-Marino; Adrian Infante-Valenzuela; Diederik Dippel; Dianne H K van Dam-Nolen; Teddy Y Wu; Martin Punter; Tajudeen Temitayo Adebayo; Abiodun H Bello; Taofiki Ajao Sunmonu; Kolawole Wasiu Wahab; Antje Sundseth; Amal M Al Hashmi; Saima Ahmad; Umair Rashid; Liliana Rodriguez-Kadota; Miguel Ángel Vences; Patrick Matic Yalung; Jon Stewart Hao Dy; Waldemar Brola; Aleksander Dębiec; Malgorzata Dorobek; Michal Adam Karlinski; Beata M Labuz-Roszak; Anetta Lasek-Bal; Halina Sienkiewicz-Jarosz; Jacek Staszewski; Piotr Sobolewski; Marcin Wiącek; Justyna Zielinska-Turek; André Pinho Araújo; Mariana Rocha; Pedro Castro; Patricia Ferreira; Ana Paiva Nunes; Luísa Fonseca; Teresa Pinho E Melo; Miguel Rodrigues; M Luis Silva; Bogdan Ciopleias; Adela Dimitriade; Cristian Falup-Pecurariu; May Adel Hamid; Narayanaswamy Venketasubramanian; Georgi Krastev; Jozef Haring; Oscar Ayo-Martin; Francisco Hernandez-Fernandez; Jordi Blasco; Alejandro Rodríguez-Vázquez; Antonio Cruz-Culebras; Francisco Moniche; Joan Montaner; Soledad Perez-Sanchez; María Jesús García Sánchez; Marta Guillán Rodríguez; Gianmarco Bernava; Manuel Bolognese; Emmanuel Carrera; Anchalee Churojana; Ozlem Aykac; Atilla Özcan Özdemir; Arsida Bajrami; Songul Senadim; Syed I Hussain; Seby John; Kailash Krishnan; Robert Lenthall; Kaiz S Asif; Kristine Below; Jose Biller; Michael Chen; Alex Chebl; Marco Colasurdo; Alexandra Czap; Adam H de Havenon; Sushrut Dharmadhikari; Clifford J Eskey; Mudassir Farooqui; Steven K Feske; Nitin Goyal; Kasey B Grimmett; Amy K Guzik; Diogo C Haussen; Majesta Hovingh; Dinesh Jillela; Peter T Kan; Rakesh Khatri; Naim N Khoury; Nicole L Kiley; Murali K Kolikonda; Stephanie Lara; Grace Li; Italo Linfante; Aaron I Loochtan; Carlos D Lopez; Sarah Lycan; Shailesh S Male; Fadi Nahab; Laith Maali; Hesham E Masoud; Jiangyong Min; Santiago Orgeta-Gutierrez; Ghada A Mohamed; Mahmoud Mohammaden; Krishna Nalleballe; Yazan Radaideh; Pankajavalli Ramakrishnan; Bliss Rayo-Taranto; Diana M Rojas-Soto; Sean Ruland; Alexis N Simpkins; Sunil A Sheth; Amy K Starosciak; Nicholas E Tarlov; Robert A Taylor; Barbara Voetsch; Linda Zhang; Hai Quang Duong; Viet-Phuong Dao; Huynh Vu Le; Thong Nhu Pham; Mai Duy Ton; Anh Duc Tran; Osama O Zaidat; Paolo Machi; Elisabeth Dirren; Claudio Rodríguez Fernández; Jorge Escartín López; Jose Carlos Fernández Ferro; Niloofar Mohammadzadeh; Neil C Suryadevara; Beatriz de la Cruz Fernández; Filipe Bessa; Nina Jancar; Megan Brady; Dawn Scozzari
Journal:  J Stroke       Date:  2022-05-31       Impact factor: 8.632

4.  Global Impact of COVID-19 on Stroke Care and IV Thrombolysis.

Authors:  Raul G Nogueira; Muhammad M Qureshi; Mohamad Abdalkader; Sheila Ouriques Martins; Hiroshi Yamagami; Zhongming Qiu; Ossama Yassin Mansour; Anvitha Sathya; Anna Czlonkowska; Georgios Tsivgoulis; Diana Aguiar de Sousa; Jelle Demeestere; Robert Mikulik; Peter Vanacker; James E Siegler; Janika Kõrv; Jose Biller; Conrad W Liang; Navdeep S Sangha; Alicia M Zha; Alexandra L Czap; Christine Anne Holmstedt; Tanya N Turan; George Ntaios; Konark Malhotra; Ashis Tayal; Aaron Loochtan; Annamarei Ranta; Eva A Mistry; Anne W Alexandrov; David Y Huang; Shadi Yaghi; Eytan Raz; Sunil A Sheth; Mahmoud H Mohammaden; Michael Frankel; Eric Guemekane Bila Lamou; Hany M Aref; Ahmed Elbassiouny; Farouk Hassan; Tarek Menecie; Wessam Mustafa; Hossam M Shokri; Tamer Roushdy; Fred S Sarfo; Tolulope Oyetunde Alabi; Babawale Arabambi; Ernest O Nwazor; Taofiki Ajao Sunmonu; Kolawole Wahab; Joseph Yaria; Haytham Hussein Mohammed; Philip B Adebayo; Anis D Riahi; Samia Ben Sassi; Lenon Gwaunza; Gift Wilson Ngwende; David Sahakyan; Aminur Rahman; Zhibing Ai; Fanghui Bai; Zhenhui Duan; Yonggang Hao; Wenguo Huang; Guangwen Li; Wei Li; Ganzhe Liu; Jun Luo; Xianjin Shang; Yi Sui; Ling Tian; Hongbin Wen; Bo Wu; Yuying Yan; Zhengzhou Yuan; Hao Zhang; Jun Zhang; Wenlong Zhao; Wenjie Zi; Thomas W Leung; Chandril Chugh; Vikram Huded; Bindu Menon; Jeyaraj Durai Pandian; P N Sylaja; Fritz Sumantri Usman; Mehdi Farhoudi; Elyar Sadeghi Hokmabadi; Anat Horev; Anna Reznik; Rotem Sivan Hoffmann; Nobuyuki Ohara; Nobuyuki Sakai; Daisuke Watanabe; Ryoo Yamamoto; Ryosuke Doijiri; Naoki Tokuda; Takehiro Yamada; Tadashi Terasaki; Yukako Yazawa; Takeshi Uwatoko; Tomohisa Dembo; Hisao Shimizu; Yuri Sugiura; Fumio Miyashita; Hiroki Fukuda; Kosuke Miyake; Junsuke Shimbo; Yusuke Sugimura; Yoshiki Yagita; Yohei Takenobu; Yuji Matsumaru; Satoshi Yamada; Ryuhei Kono; Takuya Kanamaru; Hidekazu Yamazaki; Manabu Sakaguchi; Kenichi Todo; Nobuaki Yamamoto; Kazutaka Sonoda; Tomoko Yoshida; Hiroyuki Hashimoto; Ichiro Nakahara; Aida Kondybayeva; Kamila Faizullina; Saltanat Kamenova; Murat Zhanuzakov; Jang-Hyun Baek; Yangha Hwang; Jin Soo Lee; Si Baek Lee; Jusun Moon; Hyungjong Park; Jung Hwa Seo; Kwon-Duk Seo; Sung Il Sohn; Chang Jun Young; Rechdi Ahdab; Wan Asyraf Wan Zaidi; Zariah Abdul Aziz; Hamidon Bin Basri; Law Wan Chung; Aznita Binti Ibrahim; Khairul Azmi Ibrahim; Irene Looi; Wee Yong Tan; Nafisah Wan Yahya; Stanislav Groppa; Pavel Leahu; Amal M Al Hashmi; Yahia Zakaria Imam; Naveed Akhtar; Maria Carissa Pineda-Franks; Christian Oliver Co; Dmitriy Kandyba; Adel Alhazzani; Hosam Al-Jehani; Carol Huilian Tham; Marlie Jane Mamauag; Narayanaswamy Venketasubramanian; Chih-Hao Chen; Sung-Chun Tang; Anchalee Churojana; Esref Akil; Özlem Aykaç; Atilla Ozcan Ozdemir; Semih Giray; Syed Irteza Hussain; Seby John; Huynh Le Vu; Anh Duc Tran; Huy Hoang Nguyen; Thong Nhu Pham; Thang Huy Nguyen; Trung Quoc Nguyen; Thomas Gattringer; Christian Enzinger; Monika Killer-Oberpfalzer; Flavio Bellante; Sofie De Blauwe; Geert Vanhooren; Sylvie De Raedt; Anne Dusart; Robin Lemmens; Noemie Ligot; Matthieu Pierre Rutgers; Laetitia Yperzeele; Filip Alexiev; Teodora Sakelarova; Marina Roje Bedeković; Hrvoje Budincevic; Igor Cindric; Zlatko Hucika; David Ozretic; Majda Seferovic Saric; František Pfeifer; Igor Karpowic; David Cernik; Martin Sramek; Miroslav Skoda; Helena Hlavacova; Lukas Klecka; Martin Koutny; Daniel Vaclavik; Ondrej Skoda; Jan Fiksa; Katerina Hanelova; Miroslava Nevsimalova; Robert Rezek; Petr Prochazka; Gabriela Krejstova; Jiri Neumann; Marta Vachova; Henryk Brzezanski; David Hlinovsky; Dusan Tenora; Rene Jura; Lubomír Jurák; Jan Novak; Ales Novak; Zdenek Topinka; Petr Fibrich; Helena Sobolova; Ondrej Volny; Hanne Krarup Christensen; Nicolas Drenck; Helle Klingenberg Iversen; Claus Z Simonsen; Thomas Clement Truelsen; Troels Wienecke; Riina Vibo; Katrin Gross-Paju; Toomas Toomsoo; Katrin Antsov; Francois Caparros; Charlotte Cordonnier; Maria Dan; Jean-Marc Faucheux; Laura Mechtouff; Omer Eker; Emilie Lesaine; Basile Ondze; Roxane Peres; Fernando Pico; Michel Piotin; Raoul Pop; Francois Rouanet; Tatuli Gubeladze; Mirza Khinikadze; Nino Lobjanidze; Alexander Tsiskaridze; Simon Nagel; Peter Arthur Ringleb; Michael Rosenkranz; Holger Schmidt; Annahita Sedghi; Timo Siepmann; Kristina Szabo; Götz Thomalla; Lina Palaiodimou; Dimitrios Sagris; Odysseas Kargiotis; Peter Klivenyi; Laszlo Szapary; Gabor Tarkanyi; Alessandro Adami; Fabio Bandini; Paolo Calabresi; Giovanni Frisullo; Leonardo Renieri; Davide Sangalli; Anne Pirson; Maarten Uyttenboogaart; Ido van den Wijngaard; Espen Saxhaug Kristoffersen; Waldemar Brola; Małgorzata Fudala; Ewa Horoch-Lyszczarek; Michal Karlinski; Radoslaw Kazmierski; Pawel Kram; Marcin Rogoziewicz; Rafal Kaczorowski; Piotr Luchowski; Halina Sienkiewicz-Jarosz; Piotr Sobolewski; Waldemar Fryze; Anna Wisniewska; Malgorzata Wiszniewska; Patricia Ferreira; Paulo Ferreira; Luisa Fonseca; João Pedro Marto; Teresa Pinho E Melo; Ana Paiva Nunes; Miguel Rodrigues; Vítor Tedim Cruz; Cristian Falup-Pecurariu; Georgi Krastev; Miroslav Mako; María Alonso de Leciñana; Juan F Arenillas; Oscar Ayo-Martin; Antonio Cruz Culebras; Exuperio Diez Tejedor; Joan Montaner; Soledad Pérez-Sánchez; Miguel Angel Tola Arribas; Alejandro Rodriguez Vasquez; Michael Mayza; Gianmarco Bernava; Alex Brehm; Paolo Machi; Urs Fischer; Jan Gralla; Patrik L Michel; Marios-Nikos Psychogios; Davide Strambo; Soma Banerjee; Kailash Krishnan; Joseph Kwan; Asif Butt; Luciana Catanese; Andrew M Demchuk; Thalia Field; Jennifer Haynes; Michael D Hill; Houman Khosravani; Ariane Mackey; Aleksandra Pikula; Gustavo Saposnik; Courtney Anne Scott; Ashkan Shoamanesh; Ashfaq Shuaib; Samuel Yip; Miguel A Barboza; Jose Domingo Barrientos; Ligia Ibeth Portillo Rivera; Fernando Gongora-Rivera; Nelson Novarro-Escudero; Anmylene Blanco; Michael Abraham; Diana Alsbrook; Dorothea Altschul; Anthony J Alvarado-Ortiz; Ivo Bach; Aamir Badruddin; Nobl Barazangi; Charmaine Brereton; Alicia Castonguay; Seemant Chaturvedi; Saqib A Chaudry; Hana Choe; Jae H Choi; Sushrut Dharmadhikari; Kinjal Desai; Thomas G Devlin; Vinodh T Doss; Randall Edgell; Mark Etherton; Mudassir Farooqui; Don Frei; Dheeraj Gandhi; Mikayel Grigoryan; Rishi Gupta; Ameer E Hassan; Johanna Helenius; Artem Kaliaev; Ritesh Kaushal; Priyank Khandelwal; Ayaz M Khawaja; Naim N Khoury; Benny S Kim; Dawn O Kleindorfer; Feliks Koyfman; Vivien H Lee; Lester Y Leung; Guillermo Linares; Italo Linfante; Helmi L Lutsep; Lisa Macdougall; Shailesh Male; Amer M Malik; Hesham Masoud; Molly McDermott; Brijesh P Mehta; Jiangyong Min; Manoj Mittal; Jane G Morris; Sumeet S Multani; Fadi Nahab; Krishna Nalleballe; Claude B Nguyen; Roberta Novakovic-White; Santiago Ortega-Gutierrez; Rahul H Rahangdale; Pankajavalli Ramakrishnan; Jose Rafael Romero; Natalia Rost; Aaron Rothstein; Sean Ruland; Ruchir Shah; Malveeka Sharma; Brian Silver; Marc Simmons; Abhishek Singh; Amy K Starosciak; Sheryl L Strasser; Viktor Szeder; Mohamed Teleb; Jenny P Tsai; Barbara Voetsch; Oscar Balaguera; Virginia A Pujol Lereis; Adriana Luraschi; Marcele Schettini Almeida; Fabricio Buchdid Cardoso; Adriana Conforto; Leonardo De Deus Silva; Luidia Varrone Giacomini; Fabricio Oliveira Lima; Alexandre L Longo; Pedro S C Magalhães; Rodrigo Targa Martins; Francisco Mont'alverne; Daissy Liliana Mora Cuervo; Leticia Costa Rebello; Lenise Valler; Viviane Flumignan Zetola; Pablo M Lavados; Victor Navia; Verónica V Olavarría; Juan Manuel Almeida Toro; Pablo Felipe Ricardo Amaya; Hernan Bayona; Angel Corredor; Carlos Eduardo Rivera Ordonez; Diana Katherine Mantilla Barbosa; Osvaldo Lara; Mauricio R Patiño; Luis Fernando Diaz Escobar; Donoband Edson Dejesus Melgarejo Fariña; Analia Cardozo Villamayor; Adolfo Javier Zelaya Zarza; Danny Moises Barrientos Iman; Liliana Rodriguez Kadota; Bruce Campbell; Graeme J Hankey; Casey Hair; Timothy Kleinig; Alice Ma; Rodrigo Tomazini Martins; Ramesh Sahathevan; Vincent Thijs; Daniel Salazar; Teddy Yuan-Hao Wu; Diogo C Haussen; David Liebeskind; Dileep R Yavagal; Tudor G Jovin; Osama O Zaidat; Thanh N Nguyen
Journal:  Neurology       Date:  2021-03-25       Impact factor: 11.800

5.  Lessons learned in stroke care during COVID-19 pandemic and preparing for future pandemics in the MENA+ region: A consensus statement from the MENA+-SINO.

Authors:  Amal Al Hashmi; Stephan von Bandemer; Ashfaq Shuaib; Ossama Yassin Mansour; Mohammed Wassy; Atilla Ozcan Ozdemir; Mehdi Farhoudi; Hosam Al Jehani; Adnan Khan; Seby John; Maher Saqqur
Journal:  J Neurol Sci       Date:  2021-11-27       Impact factor: 3.181

6.  Trends in Stroke Presentations before and during the COVID-19 Pandemic: A Meta-Analysis.

Authors:  Noman Ishaque; Asif Javed Butt; Joseph Kamtchum-Tatuene; Ali Zohair Nomani; Sarah Razzaq; Nida Fatima; Chetan Vekhande; Radhika Nair; Naveed Akhtar; Khurshid Khan; Maher Saqqur; Ashfaq Shuaib
Journal:  J Stroke       Date:  2022-01-31       Impact factor: 6.967

7.  Impact of COVID-19 Pandemic on Treatment Management and Clinical Outcome of Aneurysmal Subarachnoid Hemorrhage - A Single-Center Experience.

Authors:  Sepide Kashefiolasl; Lina Elisabeth Qasem; Nina Brawanski; Moritz Funke; Fee Keil; Elke Hattingen; Christian Foerch; Volker Seifert; Vincent Matthias Prinz; Marcus Czabanka; Juergen Konczalla
Journal:  Front Neurol       Date:  2022-03-21       Impact factor: 4.003

8.  The Impact of COVID-19 Pandemic on Ischemic Stroke Patients in a Comprehensive Hospital.

Authors:  Yimin Chen; Thanh N Nguyen; James E Siegler; Mohammad Mofatteh; Jack Wellington; Rongshen Yang; Lihong Zeng; Jiale Wu; Xi Sun; Daiyu Liang; Qiubi Tang; Sijie Chen; Xisheng Huang; Shuiquan Yang; Xuxing Liao
Journal:  Risk Manag Healthc Policy       Date:  2022-09-13

9.  The impact of COVID-19 on acute stroke care in Belgium.

Authors:  Vincent Raymaekers; Jelle Demeestere; Flavio Bellante; Sofie De Blauwe; Sylvie De Raedt; Anne Dusart; Lise Jodaitis; Robin Lemmens; Caroline Loos; Ligot Noémie; Matthieu P Rutgers; Fenne Vandervorst; Geert Vanhooren; Laetitia Yperzeele; Raul G Nogueira; Thanh N Nguyen; Peter Vanacker
Journal:  Acta Neurol Belg       Date:  2021-06-19       Impact factor: 2.396

10.  Safety and Outcomes of Intravenous Thrombolytic Therapy in Ischemic Stroke Patients with COVID-19: CASCADE Initiative.

Authors:  Payam Sasanejad; Leila Afshar Hezarkhani; Shahram Arsang-Jang; Georgios Tsivgoulis; Abdoreza Ghoreishi; Kristian Barlinn; Jan Rahmig; Mehdi Farhoudi; Elyar Sadeghi Hokmabadi; Afshin Borhani-Haghighi; Payam Sariaslani; Athena Sharifi-Razavi; Kavian Ghandehari; Alireza Khosravi; Craig Smith; Yongchai Nilanont; Yama Akbari; Thanh N Nguyen; Anna Bersano; Nawaf Yassi; Takeshi Yoshimoto; Simona Lattanzi; Animesh Gupta; Ramin Zand; Shahram Rafie; Seyede Pourandokht Mousavian; Mohammad Reza Shahsavaripour; Shahram Amini; Saltanat U Kamenova; Aida Kondybayeva; Murat Zhanuzakov; Elizabeth M Macri; Christa O'Hana S Nobleza; Sean Ruland; Anna M Cervantes-Arslanian; Masoom J Desai; Annemarei Ranta; Amir Moghadam Ahmadi; Mahtab Rostamihosseinkhani; Razieh Foroughi; Etrat Hooshmandi; Fahimeh H Akhoundi; Ashfaq Shuaib; David S Liebeskind; James Siegler; Jose G Romano; Stephan A Mayer; Reza Bavarsad Shahripour; Babak Zamani; Amadene Woolsey; Yasaman Fazli; Khazaei Mojtaba; Christian F Isaac; Jose Biller; Mario Di Napoli; M Reza Azarpazhooh
Journal:  J Stroke Cerebrovasc Dis       Date:  2021-09-20       Impact factor: 2.677

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