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. 2025 Jan 6:15910199241308322. Online ahead of print. doi: 10.1177/15910199241308322

The relative cerebral blood volume (rCBV) < 42% is independently associated with hemorrhagic transformation in anterior circulation large vessel occlusion

Dhairya A Lakhani 1,2,*,✉, Aneri B Balar 1,*, Subtain Ali 2, Musharaf Khan 2, Hamza A Salim 1, Manisha Koneru 3, Sijin Wen 4, Richard Wang 1, Janet Mei 1, Argye E Hillis 5, Jeremy J Heit 6, Gregory W Albers 7, Adam A Dmytriw 8, Tobias D Faizy 9, Max Wintermark 10, Kambiz Nael 11, Ansaar T Rai 2, Vivek S Yedavalli 1
PMCID: PMC11705296  PMID: 39763336

Abstract

Background

Pretreatment CT perfusion (CTP) marker relative cerebral blood volume (rCBV) < 42% lesion volume has recently shown to predict poor collateral status and poor 90-day functional outcome. However, there is a paucity of studies assessing its association with hemorrhagic transformation (HT). Here, we aim to assess the relationship between rCBV < 42% lesion volume with HT.

Methods

In this retrospective study, we included patients with acute ischemic stroke secondary to large vessel occlusion (AIS-LVO) of anterior circulation who had successful recanalization from two comprehensive stroke centers between 9/1/2017 and 10/01/2023. Successful recanalization was defined as modified treatment in cerebral infarction (mTICI) 2b or greater. Logistic regression analysis and ROC analysis were used to assess the relationship between rCBV <42% and HT.

Results

In total, 150 patients (median age: 69 years, 58.7% female) met our inclusion criteria. On multivariable logistic regression analysis, taking into account age, sex, hypertension, hyperlipidemia, diabetes, prior stroke or transient ischemic attack, admission National Institute of Health stroke scale (NIHSS), Alberta Stroke Program Early CT Score (ASPECTS), and intravenous thrombolysis, rCBV <34% (aOR:1.01, P < .05), rCBV <38% (aOR:1.01, P < .05) and rCBV <42% (aOR:1.01, P < .05) lesion volumes were independently associated with HT. On ROC analysis rCBV < 42% (AUC = 0.61, P < .05) performed slightly better than rCBV < 38% (AUC = 0.59, P < .05) and rCBV < 34% (AUC = 0.59, P < .05) in predicting HT.

Conclusion

The rCBV <42% lesion volume is independently associated with HT in AIS-LVO patients who underwent successful recanalization.

Keywords: Relative cerebral blood volume, rCBV <42%, hemorrhagic transformation

Introduction

The cerebral blood volume (CBV) provides an indirect estimate of the blood flow within the affected hemisphere of acute ischemic stroke secondary to a large vessel occlusion (AIS-LVO). 1 Hence, it is an excellent surrogate marker of collateral status (CS).

Poor collateral blood flow via pial arterial collateralization in the affected vascular territory, is associated with poor functional outcomes, unsuccessful recanalization following mechanical thrombectomy (MT) and higher rates of hemorrhagic transformation (HT).2–13 Whereas, good pial arterial collateralization has been associated with better functional outcomes, smaller infarct core, better penumbra salvage, and better recanalization following MT.2–9,13–25

The CBV within the affected hemisphere can be quantified on pretreatment CT perfusion (CTP) examination, relative to the normal cerebral hemisphere.2,26–34 The rCBV <42% volume has recently shown to predict 90-day functional outcomes, better than rCBV <34% and rCBV <38% thresholds, 35 likely attributable to its ability in better quantifying the collateral flow. Moreover, recent study have shown direct association of rCBV <42% lesion volume with the reference standard test for CS assessment, the digital subtraction angiography (DSA) derived American Society of Interventional and Therapeutic Neuroradiology (ASITN) score, 1 and with followup infarct core volume, 11 further validating rCBV < 42% as a poor prognostic marker in anterior circulation AIS-LVO patients. However, no studies have explored the association of rCBV <42% lesion volume with HT.

Hence, in this study, we aim to assess the relationship of rCBV < 42% lesion volumes with HT. We hypothesize that higher rCBV < 42% volumes are associated with HT.

Methods

Study design

The retrospective analysis of a prospectively maintained stroke databases was performed. Consecutive patients with AIS-LVO from two comprehensive stroke centers were identified from 09/01/2017 to 10/01/2023. The Johns Hopkins University institutional review board (IRB # IRB00269637) approved this study. The Strengthening the reporting of observational studies in epidemiology (STROBE) checklist guidelines for an observational study was used.

Study participants

The inclusion criteria for this study were: (a) AIS secondary to an anterior circulation LVO confirmed on CT angiography (CTA). Anterior circulation LVO was defined as occlusion of the supraclinoid internal carotid artery (ICA) segment, middle cerebral artery (MCA) M1 segment, and proximal MCA M2 segment; (b) Diagnostically adequate CT perfusion rCBV maps; (c) Those who underwent successful recanalization, defined as mTICI 2b or greater; and (d) Diagnostic adequate follow up imaging available during the same admission to detect presence of hemorrhage.

This study was performed in accordance with the Health Insurance Portability and Accountability Act (HIPAA) and Declaration of Helsinki. Informed consent was waived by the IRB given the retrospective study design. The management decisions to administer thrombolysis or to perform interventions were made on an individual basis per institutional protocols based on consensus stroke team evaluation.

Data collection

This data is prospectively collected, and the database is actively managed. The baseline and clinical data were prospectively collected through electronic records, including but not limited to baseline demographics; clinical presentation, markers of stroke diagnosis and management, markers on baseline and follow-up imaging, various time parameters, and short- and long-term follow-up data.

CTP image acquisition:

The Siemens Somatom Force (Erlangen, Germany) scanner was used. Acquisition parameters included: 70 kVP, 200 effective mAs, rotation time of 0.25 s, average acquisition time of 60 s, collimation of 48 × 1.2 mm, pitch value of 0.7, 4D range 114 mm×1.5 s.

Image analysis

The quality assessment of CT perfusion data was performed independent of the outcomes by a board certified neuroradiologists with 9 years of working experience.

The commercial RAPID perfusion software, version 5.2.2 (iSchemaView, Menlo Park, CA), was used to generate rCBV lesion volumes from raw CTP data.

Statistical analysis

The categorical data was described using contingency tables including counts and percentages; continuous variables were summarized with median (interquartile range). A student t-test was used in the data analysis for continuous variables, Mann–Whitney U test was used in the data analysis for ordinal data and Chi Square test was used for categorical data to assess differences of the variables in patients with HT and in those without.

The logistic regression and receiver operating characteristic area under the curve (ROC-AUC) analysis was used to assess the relationship between rCBV lesion volumes with dichotomized HT outcome. The Youden's Index was used to identify the best cutoff for rCBV volumes in predicting the outcome.

Multivariable logistic regression model took into account following confounding variables: age, sex, hypertension, hyperlipidemia, diabetes, prior stroke or transient ischemic attack, admission National Institute of Health stroke scale (NIHSS), Alberta Stroke Program Early CT Score (ASPECTS), and intravenous thrombolysis. Statistically significant analysis is described as P ≤ .05, P < .01 and P < .001.

Results

A total of 150 consecutive patients met our inclusion criteria. The median age of the study cohort was 69 years. A total of 86 (57%) Caucasian, and 51 (34%) African American met our inclusion criteria (Table 1). In total, 52 patients (35%) received intravenous thrombolysis (Table 1).

Table 1.

Demographics of study population, imaging biomarkers, and treatment details

No hemorrhage (n = 86) Hemorrhagic transformation (n = 64) Total (n = 150) P value
Age 70.0 (59.5–79.0) 67.0 (56.0–79.5) 69.0 (58.5–79.0) .701
Sex
 Female 56, 65.1% 32, 50.0% 88, 58.7% <.05
 Male 30, 34.9% 32, 50.0% 62, 41.3%
 Race .67
 African American 29, 33.7% 22, 34.4% 51, 34.0%
 Caucasian 51, 59.3% 35, 54.7% 86, 57.3%
 Asian 3, 3.5% 5, 7.8% 8, 5.3%
 Others 3, 3.5% 2, 3.1% 5, 3.3%
Segment Occlusion <.05
 M1 56, 65.1% 52, 81.3% 108, 72.0%
 Proximal M2 23, 26.7% 4, 6.3% 27, 18.0%
 Supraclinoid ICA 7, 8.1% 8, 12.5% 15, 10.0%
 Hypertension 70, 81.4% 49, 76.6% 119, 79.3% .68
 Smoking 43, 50.6% 32, 50.8% 75, 50.7% .40
 Alcohol 29, 34.1% 20, 31.7% 49, 33.1% .49
 Admission Body Mass Index 27.4 (23.2–33.2) 27.3 (22.8–31.2) 27.4 (23.1–32.5) .324
 Hyperlipidemia 44, 51.2% 35, 54.7% 79, 52.7% .88
 Diabetes 20, 23.3% 24, 37.5% 44, 29.3% <.05
 Coronary artery disease 49, 57.0% 32, 50.0% 81, 54.0% .94
 Atrial Fibrillation 45, 52.3% 20, 31.3% 65, 43.3% .20
 Prior Transient Ischemic Attack or stroke 14, 16.3% 15, 23.4% 29, 19.3% .61
 Intravenous thrombolysis 31, 36.0% 21, 32.8% 52, 34.7% .32
 Admission National Institute of Health stroke scale 14.0 (9.0–20.0) 16.0 (12.0–20.0) 15.0 (10.0–20.0) .366
Premorbid Modified Rankin Score .34
 0 54, 65.1% 46, 74.2% 100, 69.0%
 1 14, 16.9% 7, 11.3% 21, 14.5%
 2 5, 6.0% 5, 8.1% 10, 6.9%
 3 10, 12.0% 4, 6.5% 14, 9.7%
Alberta stroke programme early CT score (ASPECTS) .75
 0 1, 1.2% 1, 1.6% 2, 1.3%
 1 1, 1.2% 0, 0.0% 1, 0.7%
 4 0, 0.0% 1, 1.6% 1, 0.7%
 5 2, 2.3% 3, 4.7% 5, 3.3%
 6 7, 8.1% 6, 9.4% 13, 8.7%
 7 6, 7.0% 7, 10.9% 13, 8.7%
 8 15, 17.4% 8, 12.5% 23, 15.3%
 9 11, 12.8% 8, 12.5% 19, 12.7%
 10 43, 50.0% 30, 46.9% 73, 48.7%
CT Perfusion Parameters
 Tmax >6 s lesion volume 102.5 (63.0–280.0) 126.5 (81.0–288.0) 112.5 (67.0–285.0) <.001
 rCBF <30% lesion volume 0.0 (0.0–79.0) 9.5 (0.0–83.0) 5.0 (0.0–82.0) <.001
 rCBV <42% lesion volume 4.0 (0.0–64.0) 9.5 (0.0–131.0) 5.0 (0.0–94.0) <.001
 rCBV <38% lesion volume 1.5 (0.0–59.0) 7.0 (0.0–117.0) 4.5 (0.0–84.0) <.001
 rCBV <34% lesion volume 0.0 (0.0–55.0) 5.0 (0.0–110.0) 0.0 (0.0–80.0) <.001
Modified treatment in cerebral infarction (mTICI) score .54
 2b 19, 22.1% 23, 35.9% 42, 28.0%
 2c 16, 18.6% 8, 12.5% 24, 16.0%
 3 51, 59.3% 33, 51.6% 84, 56.0%
Time Parameters
 Last known well to door time (minutes) 100.5 (51.0–529.0) 69.0 (42.0–120.0) 84.0 (47.0–297.5) .06
 Door to CT time (minutes) 30.0 (17.0–45.0) 30.0 (16.0–42.0) 30.0 (17.0–45.0) .14
 Door to needle time (minutes) 65.0 (52.0–87.0) 53.0 (39.5–74.0) 59.0 (44.0–78.0) .16
 Door to groin puncture time (minutes) 165.0 (130.0–232.0) 153.0 (116.0–211.5) 156.0 (126.0–222.0) .62
 Door to recanalization time (minutes) 284.0 (204.0–570.0) 245.0 (181.0–332.0) 280.5 (193.0–407.0) .20
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Of 150 patients, 108 (72%) had M1 segment occlusion, 27 (18%) had proximal M2 segment occlusion, and 15 (10%) had supraclinoid internal carotid artery occlusion. Patient demographics, imaging parameters, and stroke treatment details are presented in Table 1.

rCBF <30% and Tmax >6 s with HT

Both rCBF <30%, and Tmax >6 s lesion volumes were significantly higher in patients with HT, compared to those without (Table 1).

However, on logistic regression analysis, rCBF < 30% (uOR: 1.01, 95%CI: 0.99–1.02, P = .10) and Tmax >6 s (uOR: 1.0, 95%CI: 1.0–1.01, P = .28) lesion volumes were not associated with HT.

rCBV <34%, rCBV <38% and rCBV <42% with HT

All three thresholds of rCBV lesion volumes were significantly higher in patients with HT, compared to those without (Table 1).

On multivariable logistic regression analysis, taking into account age, sex, hypertension, hyperlipidemia, diabetes, prior stroke or transient ischemic attack, admission NIHSS, ASPECTS, and intravenous thrombolysis, all three thresholds [rCBV <34% (aOR:1.01, P < .05), rCBV <38% (aOR:1.01, P < .05) and rCBV <42% (aOR:1.01, P < .05)] were independently associated with HT (Table 2).

Table 2.

Logistic regression analysis

uaOR (95% CI), P value Multivariable regression analysis including rCBV < 42% aOR (95% CI), P value Multivariable regression analysis including rCBV < 38% aOR (95% CI), P value Multivariable regression analysis including rCBV < 34% aOR (95% CI), P value
Age (per year) 1.00 (0.97–1.02), .66 1.00 (0.98–1.02), .95 1.00 (0.98–1.02), .95 1.00 (0.98–1.02), .95
Sex (female) 1.87 (0.96–3.61), .06 1.90 (0.92–3.90), .08 1.93 (0.94–3.96), .07 1.90 (0.92–3.90), .08
Hypertension 0.75 (0.34–1.65), .47 0.43 (0.17–1.07), .07 0.43 (0.17–1.07), .07 0.43 (0.17–1.07), .07
Hyperlipidemia 1.15 (0.60–2.20), .67 1.22 (0.59–2.51), .59 1.23 (0.60–2.54), .57 1.22 (0.59–2.51), .59
Diabetes 1.98 (0.97–4.03), .06 2.50 (1.12–5.58), <.05 2.51 (1.12–5.59), <.05 2.50 (1.12–5.58), <.05
Prior stroke or Transient Ischemic Attack 1.57 (0.70–3.55), .27 1.56 (0.64–3.76), .33 1.54 (0.64–3.73), .34 1.56 (0.64–3.76), .33
Admission National Institute of Health Stroke Scale (per point) 1.00 (0.96–1.05), .84 1.00 (0.94–1.05), .89 1.00 (0.94–1.05), .88 1.00 (0.94–1.05), .89
Alberta stroke programme early CT score (ASPECTS) (per point) 0.94 (0.79–1.11), .45 0.92 (0.76–1.11), .38 0.92 (0.76–1.11), .38 0.92 (0.76–1.11), .38
Intravenous Thrombolysis 0.87 (0.44–1.71), .68 0.80 (0.37–1.73), .56 0.80 (0.37–1.73), .56 0.80 (0.37–1.73), .56
rCBV <42% (per ml) 1.01 (1.00–1.02), <.05 1.01 (1.00–1.02), <.05
rCBV <38% (per ml) 1.01 (1.00–1.02), <.05 1.01 (1.00–1.03), <.05
rCBV < 4% (per ml) 1.01 (1.00–1.03), <.05 1.01 (1.00–1.02), <.05
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Legend: aOR = adjusted odds ratio, uaOR = unadjusted odds ratio.

On ROC analysis rCBV < 42% (AUC = 0.61, P < .05) performed marginally better than rCBV < 38% (AUC = 0.59, P < .05) and rCBV < 34% (AUC = 0.59, P < .05) in predicting HT (Figure 1). The best cutoff for rCBV <42% in predicting the outcome was 3.5 ml, where Youden's Index was maximized at 0.21. This cutoff achieved a sensitivity of 0.58 and specificity of 0.63.

Figure 1.

Figure 1.

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Receiver operating characteristic (ROC) analysis of the area under the curve (AUC) for predicting hemorrhagic transformation. The rCBV < 42% volume (AUC = 0.61, P < .05) performed slightly better than rCBV < 38% (AUC = 0.59, P < .05) and rCBV < 34% (AUC = 0.59, P < .05) in predicting hemorrhagic transformation.

Additionally, diabetes was independently associated with HT (aOR: 2.5, P < .05).

Discussion

In this study of anterior circulation AIS-LVO patients who underwent successful recanalization, we found that higher rCBV lesion volumes were independently associated with HT, and that rCBV < 42% performs slightly better than rCBV < 34% and rCBV <38% thresholds. To our knowledge, the association of rCBV <42% in estimating HT remain sparse. This study further validates rCBV < 42% as poor prognostic biomarker of HT in this patient population.

The rCBV < 42% lesion volume by definition provides an estimate of the degree of hypoperfusion in the ischemic zone, by quantifying blood volume in the ischemic territory defined by > 6 s delayed arterial transit of contrast, relative to the unaffected region. The rCBV threshold of <42% thereby provides a volume of severely hyperperfused region within the ischemic zone, thereby serving as an indirect marker of poor collateral flow.1,29,36–40 Moreover, it is well established that poor collateral flow in the ischemic territory is associated with higher rates of hemorrhagic transformation. 14 Hence, in our study the rCBV <42% lesion volume which is a great marker of poor collateral flow, was independently associated with hemorrhagic transformation.

The rCBV <42% lesion volume has shown to be associated with poor collateral status, follow-up infarct volume and 90-day functional outcomes.1,11,29,35 Moreover, review of Efficacy and safety of nerinetide for the treatment of acute ischemic stroke (ESCAPE-NA1 35 ) trial data showed that rCBV < 42% outperformed rCBV < 34% and rCBV < 38% lesion volume in predicting 90-day functional outcomes. 41 Our findings support the hypothesized physiological mechanism that a lower CBV reflects a modest degree of compensation through inadequate collateral routes and is thus associated with HT in patients with anterior circulation AIS-LVO who underwent successful recanalization. Furthermore, we observed that lesion volumes with rCBF <30% and Tmax >6 s were not associated with HT. In contrast, all three rCBV thresholds (<34%, <38%, and <42%) were associated with HT, with the rCBV <42% threshold showing slightly better performance.

Our results contradict those of McDonough et al., 42 who found that only rCBF <30% lesion volume, and not rCBV <38% or Tmax >6 s, was associated with HT. This discrepancy arises because McDonough et al. employed stringent inclusion criteria: only patients with an NIHSS >5, moderate-to-good baseline CS, ASPECTS >4, and a last-seen-well-to-door time of ≤12 h were included. They also included patients with mid- and distal-M2 segment occlusions and those with unsuccessful recanalization. Recent clinical trials have supported the use of mechanical thrombectomy (MT) in large vessel occlusion (LVO) cases regardless of core size and CS, suggesting that excluding patients with poor CS and large core (ASPECTS ≤4) may not accurately represent real-world data. Additionally, excluding patients with a prolonged last-seen-well-to-door time >12 h and those with minor strokes (NIHSS <5) limits the generalizability of the findings. Moreover, McDonough et al.'s 42 inclusion of mid- and distal-M2 occlusions, which have different management approaches compared to LVOs, and their inclusion of patients with unsuccessful recanalization attempts, who are inherently at a lower risk of HT due to failed revascularization, further contribute to the observed differences. It is important to note that authors did not study the association of rCBV <34% and rCBV <42% with HT.

The limitations of our study include the selection bias associated with retrospective analysis. Second, presence of hemorrhagic transformation was based on either CT or MR imaging at follow-up. MRI is more sensitive compared to CT in detecting hemorrhage, and hence results may favor those who underwent MR. Third, we did not take into account presence of clinically significant versus non-significant hemorrhages. 43 Fourth, the detection rate of hemorrhage is dependent on the rater, and there is modest inter- and intrarater agreement. 44 However, our strength includes prospectively derived large cohort derived from two comprehensive stroke centers.

Our results further validate the role of rCBV < 42% lesion volume in predicting HT. More recently, large core trials showed the benefit of MT in LVO cases irrespective of ischemic core volume and CS. Larger core strokes have higher odds of HT following successful recanalization. Hence, having a pretreatment marker like rCBV < 42% lesion volume that can predict HT can be used as an adjunct prognostic marker in complex cases where decision making is more nuanced. However, future studies are needed to explore the adjunct role of rCBV < 42% lesion volume in clinical evaluation and decision making for this patient population.

Acknowledgements

This study is supported by the Johns Hopkins University Department of Radiology Physician Scientist Incubator Program (RAD-PSI) to VSY and the Johns Hopkins School of Medicine Physician Scientist Scholar Program to DAL

Footnotes

Author contribution: Dhairya A. Lakhani: writing—original draft; data curation; formal analysis; investigation; methodology. Aneri B Balar: writing—original draft; formal analysis; investigation; methodology. Subtain Ali: writing—reviewing, investigation. Musharaf Khan: writing—reviewing, investigation. Hamza Salim: data curation, investigation. Manisha Koneru: data curation, investigation. Sijin Wen: formal analysis. Richard Wang: data curation. Janet Mei: data curation, data analysis. Argye E. Hillis: methodology, supervision, writing—review and editing. Jeremy J Heit: methodology, supervision, writing—review and editing. Gregory W Albers: methodology, supervision, writing—review and editing. Adam A Dmytriw MD: methodology, supervision, writing—review and editing. Tobias Faizy: methodology, supervision, writing—review and editing. Max Wintermark: methodology, supervision, writing—review and editing. Kambiz Nael: methodology, supervision, writing—review and editing. Ansaar T Rai: methodology, supervision, writing—review and editing. Vivek S Yedavalli: resources, project administration, investigation, supervision, writing—review and editing.

Data availability: The datasets used and/or analyzed during the current study available from the corresponding author on reasonable request.

Drs. Dhairya Lakhani, Greg Albers, Jeremy Heit, and Vivek Yedavalli are consultants for Rapid (iSchemaView, Menlo Park, CA).

Funding: Research reported in this publication was supported by the National Institute of General Medical Sciences of the National Institutes of Health under Award Number 5U54GM104942-08. The content is solely the responsibility of the authors and does not necessarily represent the official views of the National Institutes of Health.

IRB

Study was approved by Johns Hopkins Institutional Review Board, Reference Number IRB00269637.

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