This study observed worsened outcomes among patients with CoW anomalies, which highlights the need to include the CoW in BCVI screening and diagnostic studies. This may suggest that varying treatment is warranted for BCVI patients with concomitant CoW anomalies, but future studies are needed to confirm this. While both screening and scanning criteria for BCVI diagnoses have been well researched, there is a lack of information on screening and scanning practices that are useful for identification of CoW anomalies. There were patterns identified for both screening and scanning practices useful in identification of CoW in this study across 17 trauma centers which were not following uniform practices. Three specific BCVI screening criteria were associated with patients with CoW anomalies, and importantly, patients with CoW anomalies had a scan conducted for some other reason not currently identified as a BCVI screening criteria more often than patients with a normal CoW. Thus, current BCVI screening criteria are not inclusive of identifying co-occurring CoW anomalies. CoW anomalies were also identified more often when both the head and neck were included during the scan, rather than only one region or during a whole-body scan.
Having a complete CoW is thought to be protective of stroke as the CoW can respond to low perfusion pressure by reversing the flow providing collateralization after BCVI [17, 19, 44]. In this study a specific subset of BCVI patients with CoW anomalies were not only significantly more likely to suffer strokes, but were also more likely to have ICHs, and CSB before antithrombotic initiation than those with normal CoW anatomy. This could be a result of the altered collateral flow. This emphasizes the need to include the CoW in BCVI imaging studies and potentially the need for tailored treatment. Currently antithrombotic therapy is the frontline therapy to prevent strokes, but antithrombotic use must be balanced to consider the risk of CSB and ICH [22, 43, 45, 46]. Future studies are needed to help determine the optimal treatment for these patients, or identification of patients who would benefit from what treatment: antithrombotic or endovascular therapy. A prior study observed that the time from arrival to antithrombotic administration was significantly longer for patients who later developed an ICH, and that antithrombotic interruption was associated with a higher stroke rate [43]. Those two treatment factors may be even more important for patients with CoW anomalies. While the use of surgery is rare for BCVI, stent placement has become more common, however current indications for stenting are unclear [47]. Brommeland et al. state high grade injuries or pseudoaneurysms may be considered for endovascular therapy; evaluation of the use of endovascular therapies (stent placement, coil embolization) in patients with CoW anomalies may be warranted [14, 47]. In contrast to our findings, another study with a small sample size observed patients with normal CoW anatomy were 5.8 times more likely to have a stroke than patients with CoW anomalies [17]. Lee et al. found CoW variations in the internal carotid artery were associated with an increased risk of stroke during endovascular clamping [19]. Zhou et al. conducted a study of patients with cerebrovascular diseases and observed that having a CoW anomaly was associated with worsened National Institutes of Health Stroke Severity (NIHSS) scores when compared to having a normal CoW [48]. Another study found no difference in the rate of early neurologic events, including stroke, after carotid eversion endarterectomy when compared by presence of CoW anomalies [49]. Murphy et al. stressed the need for more studies evaluating the risks and benefits of treatment among BCVI patients, stating that delayed treatment, or no treatment may result in stroke, whereas antithrombotic therapy may result in bleeding or head injury progression among patients with BCVI [50]. Balancing the risks and benefits of antithrombotic therapy can be difficult for physicians when there is little data available, but this study was successful in identifying a specific subset patients with BCVI who may benefit from more tailored or aggressive treatment, being those with CoW anomalies, however further studies are still needed to confirm this.
Despite the fact that those with and without CoW anomalies received similar rates of antithrombotic administration during hospitalization, patients with a CoW anomaly still had higher rates of strokes, suggesting more aggressive treatment may be warranted for those with both BCVI and CoW anomalies. Furthermore, among patients with antithrombotic therapy interrupted, the stroke rate was significantly higher among patients with a CoW anomaly, whereas among those without antithrombotic interruption there was no difference in the stroke rate when compared by presence of CoW anomalies. This highlights the importance of antithrombotic therapy and may suggests that tailored treatment may be necessary to prevent strokes, which may include entail earlier antithrombotic initiation, more aggressive antithrombotic regimens, or even endovascular therapy. While the EAST guideline recommends the use of antithrombotic therapy, they state there currently is not enough data to support recommendations on the type, timing of initiation, dose, or duration of therapy [27]. WTA provides guidance that those with Grade I-IV injuries be provided low molecular weight heparin with a goal of a partial thromboplastin time of 40–50 s, stating that low molecular weight heparin is preferred as it is reversible and may be more efficacious than other antiplatelet drugs [28]. Further the WTA recommends endovascular treatment for Grade V BCVIs [28]. The Scandinavian Journal of Trauma recommends early antithrombotic treatment with heparin (50–100 IU/kg twice daily) within the first 24–48 h of diagnosis, then to transfer to oral acetyl salicylic acid (75 mg daily) and to continue treatment for at least three months [14]. They state that patients with severe luminal stenosis or progressing pseudoaneurysms should be consulted for potential endovascular therapy [14]. Future studies evaluating the efficacy of various treatment methods for patients with BCVI and CoW anomalies are needed as current guidelines do not provide recommendations for these treatments within this population.
While there was no difference in the stroke rate when compared by the anatomical region of the CoW affected in this study, those with posterior anomaly experienced more CSBs after antithrombotic initiation than those with anterior anomalies, which may indicate that those with posterior anomalies need varying antithrombotic regimens than those with anterior anomalies, such as lower antithrombotic doses, less frequent antithrombotic regimens, or increased monitoring of coagulation factors such as INR to direct treatment. In the study by Zhou et al., they found that those with posterior anomalies, or with both posterior and anterior anomalies, had significantly higher NIHSS on discharge than those with a normal CoW [48]. Shahan et al. found fetal-type enlarged persistent posterior communicating artery anomalies were associated with a trend towards a decreased stroke risk [17]. Only three patients in this study had posterior communicating artery anomalies, none of whom experienced a stroke.
Because of the association between CoW and poor outcomes, knowledge of factors associated with CoW anomalies may be useful for their identification. In this study patients with CoW anomalies had a significantly higher rate of having a prior MI and a lower rate of having pre-existing diabetes than patients with a normal CoW. In contrast to our study, another study of patients with cerebral infarctions observed that CoW anomalies were associated with an increased rate of having pre-existing diabetes when compared to patients with a normal CoW [48]. Chi et al. also studied a population of stroke patients and observed that diabetes was associated with strokes occurring specifically in the posterior vertebral basilar artery and posterior cerebral artery, rather than an infarction affecting vessels in the anterior circulation [51]. In this population of patients with BCVI, CoW anomalies occurred more frequently in the anterior arteries (n = 78) than the posterior arteries (n = 12), which may explain why these results differ from previous studies finding an higher rate of diabetes among patients with a CoW anomaly but had more anomalies in posterior vessels [48, 51]. This is the first study to our knowledge that has found an increased rate of prior MI among patients with BCVIs and CoW anomalies. In this study while diabetes and MI were significantly associated with CoW anomalies, the overall rate of diabetes (8%) and MI (< 1%) were low, and neither factor were identified as confounding variables as neither diabetes [0% – stroke in diabetics vs. 6% stroke in non-diabetics, p = 0.15] nor MI (0% -stroke among patients with prior MI vs. 5% – stroke in patients without prior MI, p > 0.99) were associated with the development of stroke in this population (data not tabulated).
Universal screening has been suggested because lengthy BCVI screening criteria are thought to be complicated and studies have found that many BCVIs (20–40%) do not meet screening criteria [9, 13, 16, 24]. Conversely, Müther et al. found 27% of BCVIs were still missed when screening all major trauma patients receiving CTAs [3]. Cook et al. reported that to identify all BCVIs, 96% of trauma patients would require screening [52]. Depending on how universal screening is implemented, some BCVIs still may be missed. Universal screening was not conducted at any of the participating centers but 38% of the index scans identifying a BCVI were conducted for trauma admission scanning, or because of some other head/neck injury not outlined as BCVI screening criteria. Furthermore, patients with CoW anomalies had scans due to some other head/neck injury not outlined as BCVI screening criteria significantly more than patients with a normal CoW. This provides evidence that expanding BCVI screening criteria to all head/neck injuries may improve diagnosis rates for both BCVI and CoW. Three BCVI scanning criteria were more common among patients with CoW anomalies (severe TBI with a GCS < 6, a complex skull fracture, or a mandible fracture); presence of these specific injuries associated with BCVI may be useful in prompting detailed imaging including the CoW to look for anomalies. However, these three criteria were notably not identified as significantly associated with the risk of stroke in this population (data not tabulated).
The CT-scanner configuration varies across guidelines; EAST recommends at least an 8-slice, Scandinavian Neurotrauma and WTA recommend at least a 16-slice, and the ACS recommends at least a 64-slice [14, 26, 27, 53]. In a meta-analysis, the sensitivity of CTAs compared with DSA did not improve when the scanner configuration was increased above 16-slice [29]. The most common scanner configuration used for the index BCVI scan and scans identifying a CoW anomaly was 64-slice. The 64-slice was available at all participating centers, and 64-slice was the highest option at seven of the 17 centers (41%); 128-slice was the highest at six centers (35%), (Supplemental Fig. 1). It appears that some centers defaulted to the highest scanner configuration available. Additionally, over time use of 16-slice significantly decreased, and use of 128-slice significantly increased (Supplemental Fig. 2). Thus, as scanners advance and higher scanner configurations are available, there may continue to be a trend in use of higher scanner configuration. While DSA is the gold standard, it is associated with higher costs and more complications than CTA, and CTA has shown comparable results in the detection of BCVI, these factors may explain why CTA was almost exclusively used in this study [3, 12, 14, 20, 26, 27, 29,30,31, 33, 34, 39]. The use of other screening modalities (MRI, MRA, and ultrasound) were very rare, and may be because prior studies found they have a lower accuracy, take longer to complete as they often require sedation, and have low sensitivity for low-grade BCVIs [6, 31, 35, 40].
Supplemental Fig. 2 describes trends in the scanner configuration use over time, summarized as proportions by the year of admission and the scanner configuration used. Symbols were used to differentiate the scanner configuration and mark the percentage of patients who had a scan during hospitalization with that corresponding scanner configuration. Linear trend lines were fitted for each scanner configuration. Asterisks next to the scanner configuration in the legend indicate a significant trend was observed over time for use of that scanner configuration. Over time there was a significant decrease in utilization of 16-slice CT (p = 0.04), and a significant increase in the utilization of 128-slice CT (p = 0.02). The use of other CT-slices [32-slice CT (p = 0.25), 64-slice CT (p = 0.80), and 512-slice CT (p = 0.86)] remained constant over time.
The region to scan for BCVI identification is not specified in the WTA or EAST guideline [27, 54]. Whereas, the ACS and the Scandinavian NeuroTrauma Guideline recommends to include the CoW by including the neck during BCVI scans [14, 26]. Hundersmarck et al. observed an increased BCVI incidence when adding the neck to their whole-body scan [2]. In this study, scans identifying a CoW anomaly were part of a whole-body scan less often than scans which did not identify a CoW anomaly. Whole-body scans are associated with false positives and undetermined grades, potentially because the patient’s arms are raised compromising the image quality [36, 55]. It is possible that scans as part of a whole-body scan may not adequately visualize the CoW as well. Scans of the head and neck only may be ideal for identification of CoW anomalies as patients with a CoW anomaly had scans of both the head and neck only significantly more often than patients with a normal CoW.
Aljuboori et al. state follow-up imaging is debated especially for high grade BCVIs which are unlikely to resolve [42]. Wu et al. observed that higher grade BCVI were more likely to have follow-up imaging but were less likely to improve than the lower grade injuries [38]. Alternatively, repeat scanning may be useful to direct treatment: antithrombotic therapy may be discontinued for resolving injuries and endovascular surgery can be considered for worsening grades [6, 42]. Future research on how repeat scans change treatment may be useful. In this study, a majority of patients with a repeat scan had no change in their grade and only 17% of patients grade worsened. Other studies have reported low rates of worsening BCVI grades (8–34%) [9, 21, 22, 42]. Progression varied by the artery involved, patients with carotid artery injuries showed changes in their grade, whereas vertebral injuries were more likely to have no change or to have an unknown progression. This may be because those with carotid artery injuries had grade I injuries (50–51%) on their index scan more often than vertebral artery injuries (36–37%). Cothren et al. also observed a high rate (78%) of grade I injuries among carotid artery BCVIs [46].
One notable finding on repeat scans was that 11% of patients had newly detected BCVIs on subsequent scans. While the BCVI grade directs treatment methods, and follow-up scans are thought to assist with treatment decisions, current guidelines do not make recommendations based on the number of arteries involved, or newly detected BCVIs appearing on subsequent scans [14, 26, 27, 53]. Future studies evaluating treatment efficacy for patients with newly detected BCVIs on subsequent scans are needed.
Limitations
This was a retrospective study with no long-term follow-up. The scans that did not identify BCVI were not collected, thus scans that missed BCVI diagnoses and completely resolved BCVIs were not summarized. Screening criteria, scanning practices, and reporting of CoW anomalies were not standardized across the seventeen participating centers with varying ACS trauma designations. In general, the higher-level trauma centers were utilizing the expanded Denver criteria, while the lower-level trauma centers had differing screening criteria or scans may have been ordered at the treating physician’s discretion. The total number of patients screened for BCVI is not known, but the frequency of BCVI among all trauma patients admitted to the Level I participating centers was 1.1% (521/47,763) and was 0.2% (40/16,969) at the Level II-IV participating trauma centers. There was variation in the scanner configuration resolutions available at each center (Supplemental Fig. 1), physicians may have used the only scanner configuration or a standardized scanner configuration rather than deciding on the scanner configuration. Contrast practices (e.g., injection rate, timing), specific descriptions of CoW anomalies (e.g. missing, aneurysms, fetal-type variations, etc.) and specific details on CSBs were not collected. There was no formal power analysis conducted for the aims examining outcomes compared by presence of CoW anomalies, which was an aim of this larger descriptive study on scanning practices for BCVI and CoW anomalies. Because of the small number of patients with a CoW anomaly, adjusted analyses to account for confounding variables were not conducted. This study was conducted within a network of American College of Surgeons accredited trauma centers located in the United States; the results may not be generalizable to other hospitals which are not accredited trauma centers, or to hospitals situated in other regions. Further the results may not be generalizable to pediatric patients, or to other centers using less advanced or differing radiological diagnosis modalities than described in this study.
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