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Use of consensus term and definition for delayed cerebral ischaemia after aneurysmal subarachnoid haemorrhage

Background and purpose - In 2010, a multidisciplinary research group proposed a consensus term and definition for the complication of delayed cerebral ischaemia (DCI) following aneurysmal subarachnoid haemorrhage (SAH). We assessed the use of this term and its definition as an endpoint in observational studies and clinical trials. Methods – Firstly, we performed a MEDLINE abstract search from Jan 2008 to Dec 2017 for observational cohort studies and clinical trials to investigate the used terminology over the years. Next, we studied trends in citations of the original paper citing the consensus definitions since publication in 2010. Results – The number of publications citing the 2010 consensus definitions has steadily increased from 18 in 2011 to 54 in 2017. Between 2010 and 2017, 527 papers were published with delayed cerebral ischemia, or another term to describe the same complication, as an endpoint. However, the term delayed cerebral ischemia was used only in 131/527 (25%) of papers and only 14/81 (17%) of clinical trials/cohort studies published in 2017 cited the consensus definitions when outlining study endpoints.


Introduction
Delayed cerebral ischaemia (DCI) is a complication that occurs in approximately 30% of patients in the first two weeks after aneurysmal subarachnoid haemorrhage (SAH). 1 Although potentially reversible, it can progress to cerebral infarction and remains the single most important cause of mortality and morbidity in those patients who survive to definitive aneurysm treatment. 2 Research into DCI has been complicated by inconsistency in the terms used to describe the phenomenon. 3 These include "cerebral vasospasm", "delayed ischaemic neurological deficit", "secondary ischaemia" and "symptomatic vasospasm" amongst many others. The major cause of this confusion arises from the combining of radiological evidence of vasoconstriction after SAH (so called "vasospasm") with the clinical features of neurological deterioration due to delayed cerebral ischaemia (DCI). Although SAH is associated with cerebral vasoconstriction 4,5 and cerebral infarction after SAH is strongly associated with poor clinical outcomes, 6,7 the exact contribution of cerebral vasoconstriction in DCI remains unclear as the two often do not co-exist. 8 In 2010 a consensus statement was published in Stroke from a multidisciplinary group of research experts which proposed a standardised term and definitions for clinical deterioration and cerebral infarction due to DCI, to be used as an endpoint in future observational studies and clinical trials of SAH (see Supplementary Material). 9 The importance of these standardised term and definitions was further emphasised through the publication of a consensus statement on the critical care management of patients with SAH in 2011. 10 We sought to quantify the effect of the publication of this standardised term and its definitions in clinical studies of SAH.

Methods
First, an electronic literature search was performed using the Medline database from January 2008 to December 2017 to investigate the used terminology in cohort studies and clinical trials over the years. The search criteria covered four terms: "subarachnoid haemorrhage", "delayed cerebral ischaemia", "vasospasm", "cerebral infarction" and "delayed ischaemic neurological deficit" with appropriate synonyms and spelling variations. To ensure complete coverage, both MeSH and free text terms were used (see Supplementary Material for full search term strategy).
Studies included were observational, cohort or clinical trials in patients with aneurysmal SAH -both prospective and retrospective studies. All publications were limited to those involving human subjects. Exclusion criteria were: 1) duplicates; 2) manuscripts not in the English language; 3) abstracts, case reports, conference presentations, editorials, meta-analyses, reviews, and expert opinions; and 4) papers specifically dealing with definitions of vasospasm, DCI etc. Identified papers were screened by title and abstract for suitability by one author (MR).
Following this, the full text of each paper selected for inclusion was reviewed. Papers were included if DCI, or another term to describe this complication, was used as an endpoint in the study. The following data were recorded from included papers:

Discussion
The results from this study demonstrate that despite the publication of standardised consensus definitions for both clinical deterioration and cerebral infarction due to DCI in 2010 by a multidisciplinary group of expert researchers, there has been poor uptake and citation of these definitions in subsequent published studies in patients with SAH. Although the number of studies using DCI as a defined endpoint has increased, there still remains a wide number of alternative terms used to describe both the clinical and radiological features investigated in studies. This continues to hamper interpretation of research into SAH due to the ongoing confusion between radiological evidence of vessel narrowing ("vasospasm") and clinical neurological deterioration due to DCI.
The recommendation from the 2010 consensus paper was that the proposed definitions "be used in future clinical trials and observational studies that have DCI as an outcome event until more accurate, reliable and sensitive tests are developed to measure DCI". 9 Whilst a lag in the inclusion of these definitions is to be expected -especially in the case of trials commenced prior to 2010 -the proportion of papers citing them has remained between 6 and 26% which is disappointing and serves to make meta-analysis or systematic review of these studies/trials extremely difficult.
Another important aspect of the consensus definitions was that the authors stressed the occurrence of clinical deterioration due to DCI be described separately from radiological or TCD evidence of cerebral vasoconstriction. As can be seen from Table 2

Conclusion
This study has highlighted the ongoing heterogeneity in terminology and definition of DCI.

Consistent use of the clear consensus definitions for both clinical deterioration and cerebral
infarction due to DCI is essential in order to collect and interpret useful data from clinical studies of patients with SAH. Authors need to be reminded that neurological deterioration due to DCI and cerebral infarction should be separated from radiological vasoconstriction when used as an endpoint for SAH research. The term "vasospasm" should be restricted to describing radiological abnormalities in blood vessels seen after SAH. Cerebral infarction remains the preferred endpoint for use in clinical trials investigating DCI after subarachnoid haemorrhage. Delayed ischaemic neurological deficit (DIND or variant