Next Article in Journal
Special Issue “New Insights into Pathophysiology, Diagnosis and Treatment of Tinnitus”
Next Article in Special Issue
Neurological Manifestations of SARS-CoV2 Infection: A Narrative Review
Previous Article in Journal
A Nomogram for Predicting the Possibility of Peripheral Neuropathy in Patients with Type 2 Diabetes Mellitus
Previous Article in Special Issue
Hospital Outcomes among COVID-19 Hospitalizations with Acute Ischemic Stroke: Cross-Sectional Study Results from California State Inpatient Database
 
 
Search for Articles:
Title / Keyword
Author / Affiliation / Email
Journal
Article Type
 
 
Advanced Search
 
Section
Special Issue
Volume
Issue
Number
Page
 
Journals
Brain Sciences
Volume 12
Issue 10
10.3390/brainsci12101327
brainsci-logo
Submit to this Journal Review for this Journal Propose a Special Issue
► Article Menu

Article Menu

share Share announcement Help format_quote Cite question_answer Discuss in SciProfiles thumb_up
...
Endorse textsms
...
Comment
first_page
settings
Order Article Reprints
Font Type:
Arial Georgia Verdana
Font Size:
Aa Aa Aa
Line Spacing:
Column Width:
Background:
Review

Subarachnoid Hemorrhage in Patients with SARS-CoV-2 Infection: Protocol for A Scoping Review

by
Amalia Cornea
1,2,
Mihaela Simu
1,2 and
Elena Cecilia Rosca
1,2,*
1
Department of Neurology, Victor Babes University of Medicine and Pharmacy Timisoara, 300041 Timișoara, Romania
2
Department of Neurology, Clinical Emergency County Hospital Timisoara, 300736 Timisoara, Romania
*
Author to whom correspondence should be addressed.
Brain Sci. 2022, 12(10), 1327; https://doi.org/10.3390/brainsci12101327
Submission received: 3 September 2022 / Revised: 22 September 2022 / Accepted: 28 September 2022 / Published: 30 September 2022
(This article belongs to the Collection COVID-19 and Brain)
Versions Notes

Abstract

:
Subarachnoid hemorrhage (SAH) is a life-threatening condition associated with high mortality and substantial long-term morbidity. The SARS-CoV-2 virus is a new pathogen that causes a disease with variable clinical manifestations. Although the Coronavirus disease 2019 (COVID-19) is associated with hypercoagulopathy, patients may also present with cerebral hemorrhage, including SAH. The present paper reports a protocol for a scoping review that is aimed to provide a comprehensive report on existing literature by examining data on SAH associated with SARS-CoV-2 infection. Our objective is to evaluate the epidemiology, clinical, laboratory, and neuroimaging features of SAH in patients with COVID-19 and to explore the etiology and possible interventions in this pathology. Using appropriate search terms, we will search LitCOVID, the WHO database on COVID-19, and MedRxiv. The inclusion criteria are pre-defined. We will extract the data of eligible studies in standardized forms and will report the results in accordance with the Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Reviews (PRISMA-ScR). We will provide information for clinicians, healthcare providers, and public health specialists.

1. Introduction

Subarachnoid hemorrhage (SAH) is a life-threatening condition resulting from the accumulation of blood between the arachnoid and the pia mater membranes. Acute bleeding into the subarachnoid space can be because of several causes. The most frequent bleeding cause is the nontraumatic spontaneous SAH. The majority of primary SAH is due to the rupture of an intracerebral aneurysm in adults or cerebral arteriovenous malformation in children. However, in adults, the patients with primary SAH may present with no evidence of cerebral aneurism or other vascular malformations (non-aneurysmal SAH) in about 10% of cases (perimesencephalic and other angiogram-negative SAH) [1,2,3,4].
The secondary SAH etiologies include trauma, the reversible cerebral vasoconstriction syndrome, posterior reversible encephalopathy syndrome (PRES), cerebral amyloid angiopathy, cerebral vasculitis, cerebral venous sinus thrombosis, coagulopathies, tumors, drugs, septic emboli from endocarditis, or iatrogenic causes [1,2].
Although SAH is a rare cause of stroke, accounting for 1–6% of all strokes [5], the patients present high mortality and substantial long-term morbidity [5,6]. Although in the past decades, the mortality rates of SAH have decreased, it remains a severe neurological problem. For example, it is estimated that 10–15% of patients die before reaching the hospital [7], and about 25% of patients die within 24 h [7,8]. In the first month, hospitalized patients have an average mortality rate of 40% [8,9,10], and approximately half of affected individuals die in the first six months. The morbidity and mortality increase with age and are dependent on the overall health status of the patient [5,6]. Among survivors, more than one-third will present major neurologic deficits. In addition, cognitive deficits were reported even in patients considered to have a good outcome [11].
The timely recognition and adequate treatment of SAH are essential, and key management recommendations include several aspects related to SAH complications [6,12]. Among complications, the most important include: hydrocephalus, rebleeding, delayed ischemia, intracerebral hemorrhage, intraventricular hemorrhage, increased intracranial pressure, seizures, left ventricular systolic dysfunction, and myocardial infarction [1,4,13].
The SARS-CoV-2 virus is a new pathogen that causes a disease with variable clinical manifestations. Although the Coronavirus disease 2019 (COVID-19) is associated with hypercoagulopathy, patients may also present with cerebral hemorrhage, including SAH, spontaneous intracerebral parenchymal hemorrhage, and diffuse petechial cerebral hemorrhage. The incidence of intracranial hemorrhage, including SAH, was reported to be 0.3–1.2% [14].
However, studies on the neurological complications of SARS-CoV-2 infection report different epidemiological data according to the COVID-19 waves. This could be due to the impact of different healthcare strategies or the virulence of the different SARS-CoV-2 strains. For example, one study reports that SAH was present in 2% of the neurological cases in the first and 4% in the second wave [15]. Interestingly, a study comparing 2086 patients with COVID-19 and ischemic stroke with a cohort of 166,586 ischemic stroke controls found that the COVID-19 patients were less likely to present hypertension, dyslipidemia, and smoking history. However, they were more likely to be male, younger, and present with diabetes, obesity, acute coronary syndrome, venous thromboembolism, acute renal failure, and comorbid intracerebral hemorrhage or SAH [16]. Compared to the years before the pandemic, the research found that there was a higher proportion of ischemic stroke and intracerebral hemorrhage but a lower percentage of SAH and transient ischemic attack among patients with SARS-CoV-2 infection [17]. In patients hospitalized with pneumonia due to COVID-19, among 1040 individuals, 79.42% presented neurological symptoms. However, cerebral hemorrhage occurred in 1.08% of patients and SAH in 0.24% [18]. In mechanically ventilated patients with COVID-19 who died, although the leading cause of death was hypoxemic respiratory failure (77.8%), cerebrovascular accident accounted for 3.2% of deaths, and SAH for 1.6% [19].
Several studies indicated a decrease in the incidences of patients with acute cerebrovascular conditions [20,21,22,23,24,25] and aneurysmal SAH [20,26,27] during the early stages of the COVID-19 pandemic. A more extensive cross-sectional study, including 49 countries and 187 centers, investigated the differences in the incidence, severity of aSAH, and the treatment modality of ruptured aneurysms during the first year of the COVID-19 pandemic comparing it with the preceding year [28]. The authors found that there were 16,247 aSAH admissions and 344,491 COVID-19 admissions, with 8300 ruptured aneurysms coiling and 4240 ruptured aneurysms clipping procedures. They report a decline in the number of aSAH admissions (−6.4%; 95%CI −7.0% to −5.8%; p = 0.0001) during 2020 compared with 2019, most pronounced in hospitals with high-volume SAH and high-volume COVID-19 cases. In addition, the authors noted a trend towards a decline in mild and moderate SAH presentations (mild: −5%; 95% CI −5.9% to –4.3%, p = 0.06; moderate: −8.3%; 95% CI −10.2% to –6.7%; p = 0.06). Nonetheless, there was no difference in higher SAH severity [28]. The study also noted a similar overall 4.1% decrease in non-traumatic SAH admission. Consequently, the authors endorse the possibility that the aSAH rates may not have been modified, but the patients were shifted to being treated at hospitals with lower-volume COVID-19 cases if high-volume hospitals were overwhelmed with patients with SARS-CoV-2 infections [28].
Hemorrhages may affect multiple organs, including the central nervous system (CNS) [29]. The pathophysiology is not yet fully elucidated, and multiple factors were implicated: microthrombosis with secondary hemorrhage, dysregulated coagulation, vascular hyperpermeability in the context of SARS-CoV-2 infection cytokine storm, endotheliitis, and vasculitis [29]. For example, the affinity of SARS-CoV-2 for angiotensin-converting enzyme 2 (ACE-2) receptors, which are expressed in endothelial and arterial smooth muscle cells in the brain, may trigger local inflammation that causes a vasculitic process. Therefore, the viral infection will damage the intracranial arteries, predisposing the vessel wall to rupture, a mechanism that could potentially explain the pathogenesis of hemorrhagic stroke [30].
In patients with COVID-19 and aneurysmal SAH, the rupture of the aneurysm was assumed to be produced due to endothelial dysfunction. In addition, as the SARS-CoV-2 downregulates the expression of the ACE-2 receptors, the disruption of the renin-angiotensin-aldosterone system may cause an uncontrolled elevation in blood pressure, which is exacerbated by preexisting hypertension; thereby, the risk of bleeding is substantially increased [31]. Some authors proposed that the hyperinflammatory state also seen in COVID-19, with hypercytokinemia and inflammation, could contribute to vascular degeneration that will lead to aneurysm formation and size or morphology change, consequently resulting in rupture and bleeding [32].
It is noteworthy that the hypothesis of an infectious cause for aneurysm rupture was rejected several decades ago. Earlier studies on the association between viral infections and SAH failed to support the hypotheses that intracranial aneurysms may develop because the initiating event of a viral infection produces any direct arterial damage, and aneurysm rupture may be temporally related to the infection [33]. The authors tested the following viruses: influenza A, influenza B, the respiratory syncytial virus (RSV), herpes simplex virus (HSV), and rubella [33].
Our objective is to evaluate the clinical, laboratory, and neuroimaging features of SAH in patients with COVID-19 and to explore the etiology and possible interventions in this pathology. We aim to provide a comprehensive report on existing literature by investigating data on SAH associated with SARS-CoV-2 infection. A scoping review will also provide an extensive perspective on SAH in patients with SARS-CoV-2 infection, revealing what other, more specific research questions can be further addressed [34]. In addition, we aim to emphasize research gaps requiring attention.

2. Materials and Methods

We will perform a scoping review as we consider it the most appropriate knowledge synthesis method that would enable us to answer our research questions [35]. We used an online tool designed to provide guidance to reviewers on methods for conducting and reporting knowledge synthesis (https://whatreviewisrightforyou.knowledgetranslation.net/) (accessed on 1 September 2022) [36].
The present review aligns with the current recommendation for scoping reviews [37,38,39,40,41]. We followed the methodological approach we used for a previous scoping review, adapted to the present research questions [34,42].
In order to identify the extent of the current research on SAH in patients with SARS-CoV-2 infection, we performed a scoping search. Our aim was to see if another systematic review had already been done, to assess whether there is enough literature available on this topic, and to develop the search terms we should use to retrieve information on our topic. We searched LitCOVID, the World Health Organization database on COVID-19 (to December 20, 2021), using the term "subarachnoid." We also searched the MedRxiv pre-print server with appropriate terms. We retrieved 468 results. After deduplication, 371 articles were included. Screening the abstracts further reduced the number of articles to 156. Finally, we identified 47 papers on SAH in patients with COVID-19, with case reports or case series. All the screening and selection of evidence in the scoping search were performed by one author and cross-checked by another reviewer. The disagreements were managed either by discussion between the two screeners or by including a third author to arbitrate.
No systematic review was published in the first two pandemic years with a specific focus on SAH. However, several systematic reviews addressed the stroke topic. For example, one review up to 23 July 2020, found that, among 275 patients with stroke and SARS-CoV-2 infection, acute intracranial bleeding was identified in 35 cases: 24 patients (68.57%) presented with intracerebral hemorrhage (ICH), four patients (11.43%) had non-traumatic SAH, and seven individuals (20%) had the simultaneously SAH and ICH [43].
Among the 47 articles identified in our scoping search, several authors report on aneurysmal SAH (aSAH) in the context of COVID-19 [31,44,45,46] and non-aneurysmal SAH. The latter type of SAH was found eighter in isolation or in the context of other associated pathologies like reversible cerebral vasoconstriction syndrome [47,48,49], cerebral venous thrombosis [50], or intraparenchymal hemorrhage [30,51].
Therefore, a scoping review on SAH associated with SARS-CoV-2 infection is timely, as it can provide valuable insights into the spectrum of this type of stroke.

2.1. Research Questions

To identify fundamental problems to be addressed, we considered several aspects of SAH in COVID-19 patients. The research questions were defined based on the Population, Concept, and Context (PCC) of the review, as recommended by the Joanna Briggs Institute [37]:
  • Is there a relationship between SARS-CoV-2 infections and the apparition of SAH?
  • If yes, what types of SAH are present in COVID-19 patients?
  • Which are the presumptive mechanisms underlying SAH?
  • What are the clinical features?
  • What do we know about laboratory and neuroimaging investigations?
  • What interventions might work?

2.2. Search Strategy and Eligible Studies

Based on our PCC mnemonic [37], we will use a broad search strategy in the following databases: LitCOVID and WHO COVID-19 database. These databases are curated for SARS-CoV-2 infection articles; therefore, we will not need to use search terms like "coronavirus" OR "COVID-19" OR "SARS-CoV-2". We will use only the keyword: "subarachnoid." LitCOVID provides access to 269627 (and growing) relevant articles in PubMed. The WHO database indexes articles from Embase, Web of Science, Scopus, ProQuest Central, grey literature, and several other databases. In addition, we will search a pre-print server (MedRxiv) using appropriate terms. MedRxiv is one of the largest repositories in medicine; currently, it has approximately 35.520 manuscripts in the health sciences domain, with 18.958 COVID-19/SARS-CoV-2 pre-prints. Search filters will not be used, as we aim to generate a comprehensive list of research. However, we will limit our included papers to English literature. Recent research indicates that excluding non-English language records from a systematic review presented only a minimal effect on results [52]. In addition, the references of the included articles will be hand-searched to identify any additional research. We will use bibliographic software (EndNote 20, Clarivate Analytics, Philadelphia, PA, USA) to store, organize, and manage all retrieved references.

2.3. Study Selection

The PCC mnemonics for the present scoping review will be: adults (over 18 years old) and children (P), with studies investigating patients with SAH (C) in the context of SARS-CoV-2 infection (C). We will include prospective or retrospective observational or interventional studies. If available, apart from primary studies, we will also include systematic reviews. There will be no restrictions on age, gender, or region.
We will include conference abstracts only if the authors did not publish a full article on the study. Conference abstracts are excluded from systematic reviews as they may not contain sufficient information for quality assessment or meta-analysis. However, we will include abstracts as they are frequently published earlier than the full articles [53], the time being essential to a rigorous review of an ongoing phenomenon.
Commentaries, correspondences, editorials, and opinion articles will be excluded. We will exclude narrative reviews, but we will assess their reference lists for possible inclusions. The inclusion and exclusion criteria are outlined in Table 1.
After the search, we will collate and upload all the identified citations into EndNote 20 (Clarivate Analytics, Philadelphia, PA, USA) and will remove all the duplicates. For the screening process, two authors will independently review the title and abstract of all identified reports, assessing the eligibility based on the criteria for inclusion and exclusion. All articles that are considered eligible by one or both reviewers will be assessed in full text. In the full-text stage, two authors will independently check, in detail, the selected articles against the inclusion criteria; in case of disagreements, a third reviewer will arbitrate. We will record and report in the final scoping review the reasons for the exclusion of papers that do not meet the inclusion criteria.
We will provide a Preferred Reporting Items for Systematic reviews and Meta-Analyses extension for Scoping Re-views (PRISMA-ScR) flow diagram with the details of the search results and included and excluded studies, presenting each stage of the study selection process [38].

2.4. Data Extraction

The results will be presented in a tabular form in order to present a descriptive summary of the finding. The extracted data will comprise specific details about the participants, the concept, and the context of the study. In addition, we will collect the following essential information: the source of the data (e.g., author, year of publication, where the study was conducted), the research methods, and findings relevant to our review questions.
The following patient data will be reported: age, gender, immunological status (vaccination, previous COVID-19 infection or immunosuppression), comorbidities and medication, clinical signs and symptoms (general and neurological), the time between the SARS-CoV-2 infection and SAH, laboratory findings (including general and specific to SARS-CoV-2 infection findings, CSF analysis), imaging (including pulmonary CT/MRI, neuroimaging and other imaging studies if performed ), postmortem investigations, type and severity of SAH, COVID-19 severity, treatment (general, and specific for COVID-19, and neurological/neurosurgical), evolution, and the assumed mechanism of SAH (See Table 2).
We will group the information into two categories for intervention studies: specific neurological or neurosurgical treatment and other interventions. We will extract data on the comparator (in available) and other details like the duration of the treatment and relevant outcomes.
In order to ensure that all relevant data is retrieved, we will produce piloted extraction forms for the first five studies. In addition, the data extraction table might be modified and revised as necessary during the data extraction stage. Therefore, we may further refine the tables. However, any modifications will be detailed in the final scoping review.
Data will be extracted independently by two reviewers; a third reviewer will solve any discrepancies. Although a formal risk of bias assessment is not planned for this scoping review, we will note the pre-prints, which have not been formally peer-reviewed.

2.5. Reporting the Results and Summarizing the Findings

The results will be presented following the PRISMA recommendations for scoping reviews [38]. We will provide a narrative summary that will accompany the tabulated or charted results. We will provide a description of how the results relate to our review’s objectives and questions. A numerical summary of the study characteristics will be presented. In addition, we will classify the findings under the main conceptual categories (e.g., clinical characteristics, paraclinical data, and interventions). We will use figures and tables to outline the results in an organized manner, in line with our objectives. We will document in the final published scoping review any amendments to this protocol, with reference to saved searches and analysis, in order to ensure a transparent process of the conduct of the review.
Finally, toward the end of the review, we will elaborate on the findings to help identify gaps in this research area.

2.6. Quality Assessment

Our main aim is to map the evidence that has been reported in the area of SAH in the context of COVID-19 disease, providing an overview of the existing literature, regardless of the risk of bias in the included studies [13]. Hence, we will not make a formal evaluation of the methodological quality of the included studies. This can be further assessed in future systematic reviews with more precise questions.

3. Discussion

Similar to other evidence synthesis methodological recommendations, the development of a protocol is a prerequisite prior to conducting a scoping review [39]. There is a growing recognition of the value of the protocols of scoping reviews, as they are an essential element that increases the value and reduces waste in research [54,55]. A prespecified protocol is important as it provides a roadmap on the direction and methodological aspects of the future review. A protocol may be seen as a recipe for a systematic review that pre-establishes the ingredients (inclusion criteria), where and how to find them (the databases to be searched and the strategy to be used), and methods. It supports the reviewers in avoiding bias as it reduces the risk of any arbitrary decisions and undesired duplication of other systematic reviews. It also fosters collaboration and enables the detection of selective reporting. In addition, it may allow the assessment and possibly feedback from the research community [39].
In the case of SAH in the context of SARS-CoV-2 infection, the most appropriate approach is a scoping review that allows for comprehensive research questions. Therefore, a descriptive presentation of the literature on this subject is the most suitable evidence-based method. It will enable us to formulate conclusions and straightforward answers to our questions and identify any research gaps in this area. The present review will provide details on key implications for future research and further need for primary studies or systematic reviews [37,56].
We will also present data on important findings that may be used to inform clinical practice. However, the implications for practice may be restricted by the fact that we will not provide a methodological quality appraisal of the included research, and the practice recommendations will not be graded [37].
We plan to discuss the results in the context of current knowledge and practice. In addition, we will also present any potential limitations of our scoping review. For example, a limitation of scoping reviews is the lack of quality appraisal. If most of the studies will include case reports with inherent biases, then outcomes like the frequency of clinical manifestations may be influenced by selective reporting of more uncommon presentations. However, case reports provide a cornerstone for learning by pattern recognition and the advancement of medical knowledge [57]. For example, a systematic review that included 172 cases of a rare disorder (glycogenic hepatopathy) enabled the characterization of patterns of liver enzymes and hepatic injury in the disease [58]. Another systematic review, including the lipodystrophy cases from the literature, warranted the proposal of core and supportive clinical features of the disease and a narrative presentation of the data on available treatment options [59]. Furthermore, case reports contain much more information on individual patients than cohort studies [60].
The strength of the scoping review will be the thorough, systematic presentation of all published literature on patients with SARS-CoV-2 infection and SAH. The results will provide valuable information for clinicians and researchers, as well as priorities for future research. Our protocol can serve as a model for other systematic reviews on neurological presentations of COVID-19 or as a model for other protocols/systematic reviews on different clinical aspects of a disease.
A possible limitation of our scoping is that we will not assess the risk of bias in the included studies. We also do not plan to perform data synthesis like a statistical meta-analysis. Meta-analyses are recommended only if the authors assessed the methodological quality or the heterogeneity of the included studies. Usually, in scoping reviews, the analysis of data is descriptive, with basic frequency analysis and percentages [39].
Ultimately, we will provide an overall conclusion based on the results, in line with our objectives and questions.

4. Conclusions

To date, several reviews on cerebrovascular events in COVID-19 patients have been published. Nonetheless, to the best of our knowledge, none of the reviews reports such a detailed presentation of SAH, covering all the critical aspects of the disease. Hence, our research will be of interest to clinicians and other healthcare providers, and public health researchers. The present work can be used as a precursor to further systematic review or meta-analysis with more circumscribed questions and may assist the development of inclusion criteria and research questions.
In addition, the publication of the present protocol enables our future scoping review of a detailed, transparent methodology. Our protocol can serve as a model for other systematic reviews on neurological presentations of COVID-19 or as a model for other protocols/systematic reviews on different clinical aspects of a disease.

Author Contributions

Conceptualization, A.C., M.S., and E.C.R.; methodology, A.C, M.S., and E.C.R.; software, A.C., E.C.R.; investigation, A.C., M.S., and E.C.R.; resources, A.C., M.S., and E.C.R.; writing—original draft preparation, A.C; writing—review and editing, A.C, M.S., and E.C.R.; visualization, A.C., M.S., and E.C.R.; supervision, M.S. and E.C.R. project administration, A.C., M.S., and E.C.R., M.S. and E.C.R. equally contributed to this manuscript, sharing the last authorship. All authors have read and agreed to the published version of the manuscript.

Funding

This research received no external funding.

Institutional Review Board Statement

Not applicable.

Informed Consent Statement

Not applicable.

Data Availability Statement

Not applicable.

Conflicts of Interest

The authors declare no conflict of interest.

References

  1. Chou, S.H. Subarachnoid Hemorrhage. Contin. Lifelong Learn. Neurol. 2021, 27, 1201–1245. [Google Scholar] [CrossRef] [PubMed]
  2. Marder, C.P.; Narla, V.; Fink, J.R.; Tozer Fink, K.R. Subarachnoid hemorrhage: Beyond aneurysms. AJR Am. J. Roentgenol. 2014, 202, 25–37. [Google Scholar] [CrossRef]
  3. Ziu, E.; Mesfin, F.B. Subarachnoid Hemorrhage. In StatPearls; StatPearls Publishing LLC.: Treasure Island, FL, USA, 2021. [Google Scholar]
  4. Macdonald, R.L.; Schweizer, T.A. Spontaneous subarachnoid haemorrhage. Lancet 2017, 389, 655–666. [Google Scholar] [CrossRef]
  5. Go, A.S.; Mozaffarian, D.; Roger, V.L.; Benjamin, E.J.; Berry, J.D.; Blaha, M.J.; Dai, S.; Ford, E.S.; Fox, C.S.; Franco, S.; et al. Heart disease and stroke statistics—2014 update: A report from the American Heart Association. Circulation 2014, 129, e28–e292. [Google Scholar] [CrossRef]
  6. Connolly, E.S., Jr.; Rabinstein, A.A.; Carhuapoma, J.R.; Derdeyn, C.P.; Dion, J.; Higashida, R.T.; Hoh, B.L.; Kirkness, C.J.; Naidech, A.M.; Ogilvy, C.S.; et al. Guidelines for the management of aneurysmal subarachnoid hemorrhage: A guideline for healthcare professionals from the American Heart Association/american Stroke Association. Stroke 2012, 43, 1711–1737. [Google Scholar] [CrossRef]
  7. Pobereskin, L.H. Incidence and outcome of subarachnoid haemorrhage: A retrospective population based study. J. Neurol. Neurosurg. Psychiatry 2001, 70, 340–343. [Google Scholar] [CrossRef]
  8. Park, S.W.; Lee, J.Y.; Heo, N.H.; Han, J.J.; Lee, E.C.; Hong, D.Y.; Lee, D.H.; Lee, M.R.; Oh, J.S. Short- and long-term mortality of subarachnoid hemorrhage according to hospital volume and severity using a nationwide multicenter registry study. Front. Neurol. 2022, 13, 952794. [Google Scholar] [CrossRef]
  9. Gouvêa Bogossian, E.; Diaferia, D.; Minini, A.; Ndieugnou Djangang, N.; Menozzi, M.; Peluso, L.; Annoni, F.; Creteur, J.; Schuind, S.; Dewitte, O.; et al. Time course of outcome in poor grade subarachnoid hemorrhage patients: A longitudinal retrospective study. BMC Neurol. 2021, 21, 196. [Google Scholar] [CrossRef] [PubMed]
  10. Lantigua, H.; Ortega-Gutierrez, S.; Schmidt, J.M.; Lee, K.; Badjatia, N.; Agarwal, S.; Claassen, J.; Connolly, E.S.; Mayer, S.A. Subarachnoid hemorrhage: Who dies, and why? Crit. Care 2015, 19, 309. [Google Scholar] [CrossRef] [PubMed]
  11. Al-Khindi, T.; Macdonald, R.L.; Schweizer, T.A. Cognitive and functional outcome after aneurysmal subarachnoid hemorrhage. Stroke 2010, 41, e519–e536. [Google Scholar] [CrossRef] [Green Version]
  12. Diringer, M.N.; Bleck, T.P.; Claude Hemphill, J., 3rd; Menon, D.; Shutter, L.; Vespa, P.; Bruder, N.; Connolly, E.S., Jr.; Citerio, G.; Gress, D.; et al. Critical care management of patients following aneurysmal subarachnoid hemorrhage: Recommendations from the Neurocritical Care Society’s Multidisciplinary Consensus Conference. Neurocrit. Care 2011, 15, 211–240. [Google Scholar] [CrossRef] [PubMed]
  13. van der Velden, L.B.; Otterspoor, L.C.; Schultze Kool, L.J.; Biessels, G.J.; Verheugt, F.W. Acute myocardial infarction complicating subarachnoid haemorrhage. Neth. Heart. J. 2009, 17, 284–287. [Google Scholar] [CrossRef]
  14. Cheruiyot, I.; Sehmi, P.; Ominde, B.; Bundi, P.; Mislani, M.; Ngure, B.; Olabu, B.; Ogeng’o, J.A. Intracranial hemorrhage in coronavirus disease 2019 (COVID-19) patients. Neurol. Sci. 2021, 42, 25–33. [Google Scholar] [CrossRef]
  15. Cristillo, V.; Pilotto, A.; Benussi, A.; Libri, I.; Giunta, M.; Morotti, A.; Gipponi, S.; Locatelli, M.; Piccinelli, S.C.; Mazzoleni, V.; et al. Clinical outcome of neurological patients with COVID-19: The impact of healthcare organization improvement between waves. Neurol. Sci. 2022, 43, 2923–2927. [Google Scholar] [CrossRef] [PubMed]
  16. de Havenon, A.; Ney, J.P.; Callaghan, B.; Delic, A.; Hohmann, S.; Shippey, E.; Esper, G.J.; Stulberg, E.; Tirschwell, D.; Frontera, J.; et al. Impact of COVID-19 on Outcomes in Ischemic Stroke Patients in the United States. J. Stroke Cerebrovasc. Dis. 2021, 30, 105535. [Google Scholar] [CrossRef]
  17. Dhamoon, M.S.; Thaler, A.; Gururangan, K.; Kohli, A.; Sisniega, D.; Wheelwright, D.; Mensching, C.; Fifi, J.T.; Fara, M.G.; Jette, N.; et al. Acute Cerebrovascular Events With COVID-19 Infection. Stroke 2021, 52, 48–56. [Google Scholar] [CrossRef] [PubMed]
  18. García, S.; Cuatepotzo-Burgos, F.M.; Toledo-Lozano, C.G.; Balderrama-Soto, A.; Alcaraz-Estrada, S.L.; Montiel-López, L.; De la Vega-Bravo, A.H.; Mondragón-Terán, P.; Santosbeña-Lagunes, M.; Escarela-Serrano, M.; et al. Neurological Manifestations and Outcomes in a Retrospective Cohort of Mexican Inpatients with SARS-CoV-2 Pneumonia: Design of a Risk Profile. Healthcare 2021, 9, 1501. [Google Scholar] [CrossRef]
  19. King, C.S.; Sahjwani, D.; Brown, A.W.; Feroz, S.; Cameron, P.; Osborn, E.; Desai, M.; Djurkovic, S.; Kasarabada, A.; Hinerman, R.; et al. Outcomes of Mechanically Ventilated Patients with COVID-19 Associated Respiratory Failure. medRxiv 2020. [Google Scholar] [CrossRef] [PubMed]
  20. Nguyen, T.N.; Haussen, D.C.; Qureshi, M.M.; Yamagami, H.; Fujinaka, T.; Mansour, O.Y.; Abdalkader, M.; Frankel, M.; Qiu, Z.; Taylor, A.; et al. Decline in subarachnoid haemorrhage volumes associated with the first wave of the COVID-19 pandemic. Stroke Vasc. Neurol. 2021, 6, 542–552. [Google Scholar] [CrossRef]
  21. Nogueira, R.G.; Qureshi, M.M.; Abdalkader, M.; Martins, S.O.; Yamagami, H.; Qiu, Z.; Mansour, O.Y.; Sathya, A.; Czlonkowska, A.; Tsivgoulis, G.; et al. Global Impact of COVID-19 on Stroke Care and IV Thrombolysis. Neurology 2021, 96, e2824–e2838. [Google Scholar] [CrossRef]
  22. Nogueira, R.G.; Abdalkader, M.; Qureshi, M.M.; Frankel, M.R.; Mansour, O.Y.; Yamagami, H.; Qiu, Z.; Farhoudi, M.; Siegler, J.E.; Yaghi, S.; et al. Global impact of COVID-19 on stroke care. Int. J. Stroke 2021, 16, 573–584. [Google Scholar] [CrossRef]
  23. Sacco, S.; Ricci, S.; Ornello, R.; Eusebi, P.; Petraglia, L.; Toni, D. Reduced Admissions for Cerebrovascular Events During COVID-19 Outbreak in Italy. Stroke 2020, 51, 3746–3750. [Google Scholar] [CrossRef]
  24. Seiffert, M.; Brunner, F.J.; Remmel, M.; Thomalla, G.; Marschall, U.; L’Hoest, H.; Acar, L.; Debus, E.S.; Blankenberg, S.; Gerloff, C.; et al. Temporal trends in the presentation of cardiovascular and cerebrovascular emergencies during the COVID-19 pandemic in Germany: An analysis of health insurance claims. Clin. Res. Cardiol. 2020, 109, 1540–1548. [Google Scholar] [CrossRef]
  25. Raymaekers, V.; Demeestere, J.; Bellante, F.; De Blauwe, S.; De Raedt, S.; Dusart, A.; Jodaitis, L.; Lemmens, R.; Loos, C.; Noémie, L.; et al. The impact of COVID-19 on acute stroke care in Belgium. Acta Neurol. Belg. 2021, 121, 1251–1258. [Google Scholar] [CrossRef]
  26. Diestro, J.D.B.; Li, Y.M.; Parra-Fariñas, C.; Sarma, D.; Bharatha, A.; Marotta, T.R.; Spears, J. Letter to the Editor ‘Aneurysmal Subarachnoid Hemorrhage: Collateral Damage of COVID?’. World Neurosurg. 2020, 139, 744–745. [Google Scholar] [CrossRef] [PubMed]
  27. Bernat, A.L.; Giammattei, L.; Abbritti, R.; Froelich, S. Impact of COVID-19 pandemic on subarachnoid hemorrhage. J. Neurosurg. Sci. 2020, 64, 409–410. [Google Scholar] [CrossRef]
  28. Global impact of the COVID-19 pandemic on subarachnoid haemorrhage hospitalisations, aneurysm treatment and in-hospital mortality: 1-year follow-up. J. Neurol. Neurosurg. Psychiatry 2022, 93, 1028–1038. [CrossRef] [PubMed]
  29. Harrogate, S.; Mortimer, A.; Burrows, L.; Fiddes, B.; Thomas, I.; Rice, C.M. Non-aneurysmal subarachnoid haemorrhage in COVID-19. Neuroradiology 2021, 63, 149–152. [Google Scholar] [CrossRef] [PubMed]
  30. Chua, A.M.U.; Jamora, R.D.G.; Jose, A.C.E.; Anlacan, V.M.M. Cerebral Vasculitis in a COVID-19 Confirmed Postpartum Patient: A Case Report. Case Rep. Neurol. 2021, 13, 324–328. [Google Scholar] [CrossRef]
  31. Abbas, R.; El Naamani, K.; Sweid, A.; Schaefer, J.W.; Bekelis, K.; Sourour, N.; Elhorany, M.; Pandey, A.S.; Tjoumakaris, S.; Gooch, M.R.; et al. Intracranial Hemorrhage in Patients with Coronavirus Disease 2019 (COVID-19): A Case Series. World Neurosurg. 2021, 154, e473–e480. [Google Scholar] [CrossRef]
  32. Fiani, B.; Fowler, J.B.; Figueras, R.A.; Hessamian, K.; Mercado, N.; Vukcevich, O.; Singh, M.K. Ruptured cerebral aneurysms in COVID-19 patients: A review of literature with case examples. Surg. Neurol. Int. 2021, 12, 187. [Google Scholar] [CrossRef]
  33. Timmons, T.A.; Donnan, G.A.; Whisnant, J.P.; Shelley, C.D.; Smith, T.F. Aneurysmal subarachnoid hemorrhage and viral infection. Lack of association. Arch. Neurol. 1986, 43, 376–378. [Google Scholar] [CrossRef]
  34. Rosca, E.C.; Tudor, R.; Cornea, A.; Simu, M. Parkinson’s Disease in Romania: A Scoping Review Protocol. Brain Sci. 2021, 11, 251. [Google Scholar] [CrossRef] [PubMed]
  35. Tricco, A.C.; Zarin, W.; Ghassemi, M.; Nincic, V.; Lillie, E.; Page, M.J.; Shamseer, L.; Antony, J.; Rios, P.; Hwee, J.; et al. Same family, different species: Methodological conduct and quality varies according to purpose for five types of knowledge synthesis. J. Clin. Epidemiol. 2018, 96, 133–142. [Google Scholar] [CrossRef]
  36. Munn, Z.; Peters, M.D.J.; Stern, C.; Tufanaru, C.; McArthur, A.; Aromataris, E. Systematic review or scoping review? Guidance for authors when choosing between a systematic or scoping review approach. BMC Med. Res. Methodol. 2018, 18, 143. [Google Scholar] [CrossRef]
  37. Peters, M.; Godfrey, C.; McInerney, P.; Munn, Z.; Tricco, A.; Khalil, H. Chapter 11: Scoping Reviews (2020 Version). Available online: https://jbi-global-wiki.refined.site/space/MANUAL/3283910770/Chapter+11%3A+Scoping+reviews (accessed on 22 December 2021).
  38. Tricco, A.C.; Lillie, E.; Zarin, W.; O’Brien, K.K.; Colquhoun, H.; Levac, D.; Moher, D.; Peters, M.D.J.; Horsley, T.; Weeks, L.; et al. PRISMA Extension for Scoping Reviews (PRISMA-ScR): Checklist and Explanation. Ann. Intern. Med. 2018, 169, 467–473. [Google Scholar] [CrossRef] [PubMed]
  39. Peters, M.D.J.; Godfrey, C.; McInerney, P.; Khalil, H.; Larsen, P.; Marnie, C.; Pollock, D.; Tricco, A.C.; Munn, Z. Best practice guidance and reporting items for the development of scoping review protocols. JBI Evid. Synth. 2022, 20, 953–968. [Google Scholar] [CrossRef]
  40. Wong, G.K.; Lam, S.W.; Wong, A.; Mok, V.; Siu, D.; Ngai, K.; Poon, W.S. Early MoCA-assessed cognitive impairment after aneurysmal subarachnoid hemorrhage and relationship to 1-year functional outcome. Transl. Stroke Res. 2014, 5, 286–291. [Google Scholar] [CrossRef] [PubMed]
  41. Peters, M.D.J.; Marnie, C.; Tricco, A.C.; Pollock, D.; Munn, Z.; Alexander, L.; McInerney, P.; Godfrey, C.M.; Khalil, H. Updated methodological guidance for the conduct of scoping reviews. JBI Evid. Synth. 2020, 18, 2119–2126. [Google Scholar] [CrossRef]
  42. Rosca, E.C.; Tudor, R.; Cornea, A.; Simu, M. Parkinson’s Disease in Romania: A Scoping Review. Brain Sci. 2021, 11, 709. [Google Scholar] [CrossRef]
  43. Fraiman, P.; Godeiro Junior, C.; Moro, E.; Cavallieri, F.; Zedde, M. COVID-19 and Cerebrovascular Diseases: A Systematic Review and Perspectives for Stroke Management. Front. Neurol. 2020, 11, 574694. [Google Scholar] [CrossRef] [PubMed]
  44. Al Saiegh, F.; Ghosh, R.; Leibold, A.; Avery, M.B.; Schmidt, R.F.; Theofanis, T.; Mouchtouris, N.; Philipp, L.; Peiper, S.C.; Wang, Z.-X.; et al. Status of SARS-CoV-2 in cerebrospinal fluid of patients with COVID-19 and stroke. J. Neurol. Neurosurg. Psychiatry 2020, 91, 846–848. [Google Scholar] [CrossRef] [PubMed]
  45. Batcik, O.E.; Kanat, A.; Cankay, T.U.; Ozturk, G.; Kazancioglu, L.; Kazdal, H.; Gundogdu, H.; Ozdemir, B.; Bahceci, I.; Kostakoglu, U.; et al. COVID-19 infection produces subarachnoid hemorrhage; acting now to understand its cause: A short communication. Clin. Neurol. Neurosurg. 2021, 202, 106495. [Google Scholar] [CrossRef]
  46. Cezar-Junior, A.B.; Faquini, I.V.; Silva, J.L.J.; de Carvalho Junior, E.V.; Lemos, L.E.A.S.; Freire Filho, J.B.M.; de Lira Filho, H.T.; Pontes, E.C.d.A.; Almeida, N.S.; Azevedo-Filho, H.R.C. Subarachnoid hemorrhage and COVID-19: Association or coincidence? Medicine 2020, 99, e23862. [Google Scholar] [CrossRef] [PubMed]
  47. Dakay, K.; Kaur, G.; Gulko, E.; Santarelli, J.; Bowers, C.; Mayer, S.A.; Gandhi, C.D.; Al-Mufti, F. Reversible cerebral vasoconstriction syndrome and dissection in the setting of COVID-19 infection. J. Stroke Cerebrovasc. Dis. 2020, 29, 105011. [Google Scholar] [CrossRef] [PubMed]
  48. Al-Mufti, F.; Becker, C.; Kamal, H.; Alshammari, H.; Dodson, V.; Nuoman, R.; Dakay, K.; Cooper, J.; Gulko, E.; Kaur, G.; et al. Acute Cerebrovascular Disorders and Vasculopathies Associated with Significant Mortality in SARS-CoV-2 Patients Admitted to The Intensive Care Unit in The New York Epicenter. J. Stroke Cerebrovasc. Dis. 2021, 30, 105429. [Google Scholar] [CrossRef]
  49. Arandela, K.; Samudrala, S.; Abdalkader, M.; Anand, P.; Daneshmand, A.; Dasenbrock, H.; Nguyen, T.; Ong, C.; Takahashi, C.; Shulman, J.; et al. Reversible Cerebral Vasoconstriction Syndrome in Patients with Coronavirus Disease: A Multicenter Case Series. J. Stroke Cerebrovasc. Dis. 2021, 30, 106118. [Google Scholar] [CrossRef]
  50. Beretta, S.; Da Re, F.; Francioni, V.; Remida, P.; Storti, B.; Fumagalli, L.; Piatti, M.L.; Santoro, P.; Cereda, D.; Cutellè, C.; et al. Case Report: Concomitant Massive Cerebral Venous Thrombosis and Internal Iliac Vein Thrombosis Related to Paucisymptomatic COVID-19 Infection. Front. Neurol. 2021, 12, 622130. [Google Scholar] [CrossRef]
  51. Bradley, B.T.; Maioli, H.; Johnston, R.; Chaudhry, I.; Fink, S.L.; Xu, H.; Najafian, B.; Marshall, D.; Lacy, J.M.; Williams, T.; et al. Histopathology and Ultrastructural Findings of Fatal COVID-19 Infections. medRxiv 2020. [Google Scholar] [CrossRef]
  52. Nussbaumer-Streit, B.; Klerings, I.; Dobrescu, A.I.; Persad, E.; Stevens, A.; Garritty, C.; Kamel, C.; Affengruber, L.; King, V.J.; Gartlehner, G. Excluding non-English publications from evidence-syntheses did not change conclusions: A meta-epidemiological study. J. Clin. Epidemiol. 2020, 118, 42–54. [Google Scholar] [CrossRef]
  53. Scherer, R.W.; Saldanha, I.J. How should systematic reviewers handle conference abstracts? A view from the trenches. Syst. Rev. 2019, 8, 264. [Google Scholar] [CrossRef]
  54. Moher, D.; Glasziou, P.; Chalmers, I.; Nasser, M.; Bossuyt, P.M.M.; Korevaar, D.A.; Graham, I.D.; Ravaud, P.; Boutron, I. Increasing value and reducing waste in biomedical research: Who’s listening? Lancet 2016, 387, 1573–1586. [Google Scholar] [CrossRef]
  55. Shamseer, L.; Moher, D.; Clarke, M.; Ghersi, D.; Liberati, A.; Petticrew, M.; Shekelle, P.; Stewart, L.A. Preferred reporting items for systematic review and meta-analysis protocols (PRISMA-P) 2015: Elaboration and explanation. BMJ 2015, 350, g7647. [Google Scholar] [CrossRef] [PubMed]
  56. Khalil, H.; Peters, M.D.; Tricco, A.C.; Pollock, D.; Alexander, L.; McInerney, P.; Godfrey, C.M.; Munn, Z. Conducting high quality scoping reviews-challenges and solutions. J. Clin. Epidemiol. 2021, 130, 156–160. [Google Scholar] [CrossRef]
  57. Murad, M.H.; Sultan, S.; Haffar, S.; Bazerbachi, F. Methodological quality and synthesis of case series and case reports. BMJ Evid.-Based Med. 2018, 23, 60–63. [Google Scholar] [CrossRef]
  58. Bazerbachi, F.; Haffar, S.; Leise, M.D.; Sharma, A.; Mukewar, S.; Sugihara, T.; Murad, M.H.; Watt, K.D. Liver function tests and pattern of hepatic injury in glycogenic hepatopathy associated with insulin-dependent diabetes mellitus: A systematic review and analysis of 172 cases. Hepatology 2017, 66 (Suppl. 1), 441A. [Google Scholar] [CrossRef]
  59. Gupta, N.; Asi, N.; Farah, W.; Almasri, J.; Barrionuevo, P.; Alsawas, M.; Wang, Z.; Haymond, M.W.; Brown, R.J.; Murad, M.H. Clinical Features and Management of Non-HIV–Related Lipodystrophy in Children: A Systematic Review. J. Clin. Endocrinol. Metab. 2017, 102, 363–374. [Google Scholar] [CrossRef]
  60. Rosca, E.C.; Tudor, R.; Cornea, A.; Simu, M. Central Nervous System Involvement in Trichinellosis: A Systematic Review. Diagnostics 2021, 11, 945. [Google Scholar] [CrossRef]
Table
Table 1. Inclusion and exclusion criteria.
Table 1. Inclusion and exclusion criteria.
Inclusion CriteriaExclusion Criteria
PopulationAdults and childrenN/A
ConceptSubarachnoid hemorrhage (SAH)Patients without SAH
Traumatic SAH
ContextSARS-CoV-2 infectionNo SARS-CoV-2 infection
Study typeCase report, case series, cohort studiesN/A
Prospective, retrospectiveN/A
Observational, interventionalPredictive modeling
Systematic reviewNarrative review
Original researchCommentaries, correspondences, editorials, opinion articles
LanguageEnglishNon-English
YearFrom 2019Before 2019
Table
Table 2. Data extraction form.
Table 2. Data extraction form.
DimensionsDetails
General informationAuthors, year, country
Study characteristicsType of study
Study participantsNumber
Age
Gender
Immunological status (vaccination, previous COVID-19 infection, or immunosuppression)
Comorbidities and medication
General clinical signs and symptoms
Neurological signs and symptoms
Time between SARS-CoV-2 infection and SAH
Laboratory findingsSARS-CoV-2 diagnosis
General laboratory findings
CSF analysis
Imaging dataPulmonary imaging
Neuroimaging
Other imaging
Postmortem dataPostmortem examination
Type of SAHAneurysmal SAH/non-aneurysmal SAH
SAH severityHunt and Hess grade, World Federation of Neurosurgical Societies, Fisher grade, etc.
COVID-19 severityMild, medium, or severe
InterventionSpecific neurological/neurosurgical treatment
COVID-19 treatment
Other treatments/general treatment
Evolution Outcome
Modified Rankin Scale
Assumed mechanism of SAH
Additional comments/notes
Publisher’s Note: MDPI stays neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Share and Cite

MDPI and ACS Style

Cornea, A.; Simu, M.; Rosca, E.C. Subarachnoid Hemorrhage in Patients with SARS-CoV-2 Infection: Protocol for A Scoping Review. Brain Sci. 2022, 12, 1327. https://doi.org/10.3390/brainsci12101327

AMA Style

Cornea A, Simu M, Rosca EC. Subarachnoid Hemorrhage in Patients with SARS-CoV-2 Infection: Protocol for A Scoping Review. Brain Sciences. 2022; 12(10):1327. https://doi.org/10.3390/brainsci12101327

Chicago/Turabian Style

Cornea, Amalia, Mihaela Simu, and Elena Cecilia Rosca. 2022. "Subarachnoid Hemorrhage in Patients with SARS-CoV-2 Infection: Protocol for A Scoping Review" Brain Sciences 12, no. 10: 1327. https://doi.org/10.3390/brainsci12101327

Note that from the first issue of 2016, this journal uses article numbers instead of page numbers. See further details here.

Article Metrics

Back to TopTop