Association Between Hematoma Expansion Severity and Outcome and Its Interaction With Baseline Intracerebral Hemorrhage Volume

Andrea Morotti¹, Gregoire Boulouis², Jawed Nawabi², Qi Li², Andreas Charidimou², Marco Pasi², Frieder Schlunk², Ashkan Shoamanesh², Aristeidis H Katsanos², Federico Mazzacane², Giorgio Busto², Francesco Arba², Laura Brancaleoni², Sebastiano Giacomozzi², Luigi Simonetti², Andrew D Warren², Michele Laudisi², Anna Cavallini², M Edip Gurol², Anand Viswanathan², Andrea Zini², Ilaria Casetta², Enrico Fainardi², Steven M Greenberg², Alessandro Padovani², Jonathan Rosand², Joshua N Goldstein²

Affiliations

¹ From the Neurology Unit (A.M.), Department of Neurological Sciences and Vision, ASST-SpedaliCivili, Brescia, Italy; Neuroradiology Department (G. Boulouis), University Hospital of Tours, CEDEX 09, France; Department of Radiology (CCM) (J.N.), Charité-Universitätsmedizin Berlin, Campus Mitte, Humboldt-Universität zu Berlin, Freie Universität Berlin, Berlin Institute of Health; Berlin Institute of Health (BIH) (J.N., F.S.), BIH Biomedical Innovation Academy, Germany; Department of Neurology (Q.L.), The First Affiliated Hospital of Chongqing Medical University; Department of Neurology (Q.L.), The Second Affiliated Hospital of Anhui Medical University, Hefei, China; Department of Neurology (A. Charidimou), Boston University Medical Center and Boston University School of Medicine, MA; Neurology Department (M.P.), University Hospital of Tours, CEDEX 09, France; Department of Neuroradiology (F.S.), Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Division of Neurology (A.S., A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; U.O. Neurologia d'Urgenza e Stroke Unit (F.M., A. Cavallini), IRCCS Fondazione Mondino, Pavia; Department of Biomedical Experimental and Clinical Neuroradiology (G. Busto, E.F.), University of Firenze, AOU Careggi; Stroke Unit (F.A.), AOU Careggi, Firenze; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.B., S.G., A.Z.),UOC Neurologia e Rete Stroke Metropolitana, Ospedale Maggiore; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.S.), Unità di Neuroradiologia, Ospedale Maggiore, Italy; J.P. Kistler Stroke Research Center (A.D.W., M.E.G., A.V., S.M.G., J.R., J.N.G.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston; Clinica Neurologica (M.L., I.C.), Dipartimento di Scienze Biomediche e Chirurgico Specialistiche, Università degli studi di Ferrara, Ospedale Universitario S. Anna, Ferrara; Department of Clinical and Experimental Sciences (A.P.), Neurology Unit, University of Brescia, Italy; Division of Neurocritical Care and Emergency Neurology (J.R.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; and Henry and Allison McCance Center for Brain Health (J.R., J.N.G.), and Department of Emergency Medicine (J.N.G.), Massachusetts General Hospital, Boston. andrea.morotti85@gmail.com.
² From the Neurology Unit (A.M.), Department of Neurological Sciences and Vision, ASST-SpedaliCivili, Brescia, Italy; Neuroradiology Department (G. Boulouis), University Hospital of Tours, CEDEX 09, France; Department of Radiology (CCM) (J.N.), Charité-Universitätsmedizin Berlin, Campus Mitte, Humboldt-Universität zu Berlin, Freie Universität Berlin, Berlin Institute of Health; Berlin Institute of Health (BIH) (J.N., F.S.), BIH Biomedical Innovation Academy, Germany; Department of Neurology (Q.L.), The First Affiliated Hospital of Chongqing Medical University; Department of Neurology (Q.L.), The Second Affiliated Hospital of Anhui Medical University, Hefei, China; Department of Neurology (A. Charidimou), Boston University Medical Center and Boston University School of Medicine, MA; Neurology Department (M.P.), University Hospital of Tours, CEDEX 09, France; Department of Neuroradiology (F.S.), Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Division of Neurology (A.S., A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; U.O. Neurologia d'Urgenza e Stroke Unit (F.M., A. Cavallini), IRCCS Fondazione Mondino, Pavia; Department of Biomedical Experimental and Clinical Neuroradiology (G. Busto, E.F.), University of Firenze, AOU Careggi; Stroke Unit (F.A.), AOU Careggi, Firenze; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.B., S.G., A.Z.),UOC Neurologia e Rete Stroke Metropolitana, Ospedale Maggiore; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.S.), Unità di Neuroradiologia, Ospedale Maggiore, Italy; J.P. Kistler Stroke Research Center (A.D.W., M.E.G., A.V., S.M.G., J.R., J.N.G.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston; Clinica Neurologica (M.L., I.C.), Dipartimento di Scienze Biomediche e Chirurgico Specialistiche, Università degli studi di Ferrara, Ospedale Universitario S. Anna, Ferrara; Department of Clinical and Experimental Sciences (A.P.), Neurology Unit, University of Brescia, Italy; Division of Neurocritical Care and Emergency Neurology (J.R.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; and Henry and Allison McCance Center for Brain Health (J.R., J.N.G.), and Department of Emergency Medicine (J.N.G.), Massachusetts General Hospital, Boston.

PMID: 37604661
PMCID: PMC10585678
DOI: 10.1212/WNL.0000000000207728

Association Between Hematoma Expansion Severity and Outcome and Its Interaction With Baseline Intracerebral Hemorrhage Volume

Andrea Morotti et al. Neurology. 2023.

. 2023 Oct 17;101(16):e1606-e1613.

doi: 10.1212/WNL.0000000000207728. Epub 2023 Aug 21.

Authors

Affiliations

¹ From the Neurology Unit (A.M.), Department of Neurological Sciences and Vision, ASST-SpedaliCivili, Brescia, Italy; Neuroradiology Department (G. Boulouis), University Hospital of Tours, CEDEX 09, France; Department of Radiology (CCM) (J.N.), Charité-Universitätsmedizin Berlin, Campus Mitte, Humboldt-Universität zu Berlin, Freie Universität Berlin, Berlin Institute of Health; Berlin Institute of Health (BIH) (J.N., F.S.), BIH Biomedical Innovation Academy, Germany; Department of Neurology (Q.L.), The First Affiliated Hospital of Chongqing Medical University; Department of Neurology (Q.L.), The Second Affiliated Hospital of Anhui Medical University, Hefei, China; Department of Neurology (A. Charidimou), Boston University Medical Center and Boston University School of Medicine, MA; Neurology Department (M.P.), University Hospital of Tours, CEDEX 09, France; Department of Neuroradiology (F.S.), Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Division of Neurology (A.S., A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; U.O. Neurologia d'Urgenza e Stroke Unit (F.M., A. Cavallini), IRCCS Fondazione Mondino, Pavia; Department of Biomedical Experimental and Clinical Neuroradiology (G. Busto, E.F.), University of Firenze, AOU Careggi; Stroke Unit (F.A.), AOU Careggi, Firenze; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.B., S.G., A.Z.),UOC Neurologia e Rete Stroke Metropolitana, Ospedale Maggiore; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.S.), Unità di Neuroradiologia, Ospedale Maggiore, Italy; J.P. Kistler Stroke Research Center (A.D.W., M.E.G., A.V., S.M.G., J.R., J.N.G.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston; Clinica Neurologica (M.L., I.C.), Dipartimento di Scienze Biomediche e Chirurgico Specialistiche, Università degli studi di Ferrara, Ospedale Universitario S. Anna, Ferrara; Department of Clinical and Experimental Sciences (A.P.), Neurology Unit, University of Brescia, Italy; Division of Neurocritical Care and Emergency Neurology (J.R.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; and Henry and Allison McCance Center for Brain Health (J.R., J.N.G.), and Department of Emergency Medicine (J.N.G.), Massachusetts General Hospital, Boston. andrea.morotti85@gmail.com.
² From the Neurology Unit (A.M.), Department of Neurological Sciences and Vision, ASST-SpedaliCivili, Brescia, Italy; Neuroradiology Department (G. Boulouis), University Hospital of Tours, CEDEX 09, France; Department of Radiology (CCM) (J.N.), Charité-Universitätsmedizin Berlin, Campus Mitte, Humboldt-Universität zu Berlin, Freie Universität Berlin, Berlin Institute of Health; Berlin Institute of Health (BIH) (J.N., F.S.), BIH Biomedical Innovation Academy, Germany; Department of Neurology (Q.L.), The First Affiliated Hospital of Chongqing Medical University; Department of Neurology (Q.L.), The Second Affiliated Hospital of Anhui Medical University, Hefei, China; Department of Neurology (A. Charidimou), Boston University Medical Center and Boston University School of Medicine, MA; Neurology Department (M.P.), University Hospital of Tours, CEDEX 09, France; Department of Neuroradiology (F.S.), Charité-Universitätsmedizin Berlin, corporate member of Freie Universität Berlin, Humboldt-Universität zu Berlin, Germany; Division of Neurology (A.S., A.H.K.), McMaster University/Population Health Research Institute, Hamilton, Ontario, Canada; U.O. Neurologia d'Urgenza e Stroke Unit (F.M., A. Cavallini), IRCCS Fondazione Mondino, Pavia; Department of Biomedical Experimental and Clinical Neuroradiology (G. Busto, E.F.), University of Firenze, AOU Careggi; Stroke Unit (F.A.), AOU Careggi, Firenze; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.B., S.G., A.Z.),UOC Neurologia e Rete Stroke Metropolitana, Ospedale Maggiore; IRCCS Istituto delle Scienze Neurologiche di Bologna (L.S.), Unità di Neuroradiologia, Ospedale Maggiore, Italy; J.P. Kistler Stroke Research Center (A.D.W., M.E.G., A.V., S.M.G., J.R., J.N.G.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School, Boston; Clinica Neurologica (M.L., I.C.), Dipartimento di Scienze Biomediche e Chirurgico Specialistiche, Università degli studi di Ferrara, Ospedale Universitario S. Anna, Ferrara; Department of Clinical and Experimental Sciences (A.P.), Neurology Unit, University of Brescia, Italy; Division of Neurocritical Care and Emergency Neurology (J.R.), Department of Neurology, Massachusetts General Hospital, Harvard Medical School; and Henry and Allison McCance Center for Brain Health (J.R., J.N.G.), and Department of Emergency Medicine (J.N.G.), Massachusetts General Hospital, Boston.

PMID: 37604661
PMCID: PMC10585678
DOI: 10.1212/WNL.0000000000207728

Abstract

Background and objectives: Hematoma expansion (HE) is a major determinant of neurologic deterioration and poor outcome in intracerebral hemorrhage (ICH) and represents an appealing therapeutic target. We analyzed the prognostic effect of different degrees of HE.

Methods: This was a retrospective analysis of patients with ICH admitted at 8 academic institutions in Italy, Germany, Canada, China, and the United States. All patients underwent baseline and follow-up imaging for HE assessment. Relative HE (rHE) was classified as follows: none (<0%), mild (0%-33%), moderate (33.1%-66%), and severe (>66%). Absolute HE (aHE) was classified as none (<0 mL), mild (0-6.0 mL), moderate (6.1-12.5 mL), and severe (>12.5 mL). Predictors of poor functional outcome (90 days modified Rankin Scale 4-6) were explored with logistic regression.

Results: We included 2,163 patients, of whom 1,211 (56.0%) had poor outcome. The occurrence of severe aHE or rHE was more common in patients with unfavorable outcome (13.9% vs 6.5%, p < 0.001 and 18.3% vs 7.2%, p < 0.001 respectively). This association was confirmed in logistic regression (rHE odds ratio [OR] 1.98, 95% CI 1.38-2.82, p < 0.001; aHE OR 1.73, 95% CI 1.23-2.45, p = 0.002) while there was no association between mild or moderate HE and poor outcome. The association between severe HE and poor outcome was significant only in patients with baseline ICH volume below 30 mL.

Discussion: The strongest association between HE and outcome was observed in patients with smaller initial volume experiencing severe HE. These findings may inform clinical trial design and guide clinicians in selecting patients for antiexpansion therapies.

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Conflict of interest statement

A.H. Katsanos is supported from a McMaster University Department of Medicine Career Research Award. J. Rosand receives research support from NIH and the American Heart Association. He has consulted with Takeda and the National Football League. J.N. Goldstein has received research support from NIH, Pfizer, Takeda, and Octapharma. He has received consulting support from Astrazeneca, CSL Behring, NControl, and Cayuga. All other authors report no relevant disclosures. Go to Neurology.org/N for full disclosures.

Figures

**Figure 1. Selection Flowchart**
ICH = intracerebral hemorrhage.

**Figure 2. Illustrative Example of Different Degrees of Hematoma Expansion**
Baseline and follow-up imaging in patients with no (A), mild (B), moderate (C), and severe (D) hematoma expansion.

**Figure 3. Predicted Probability of Poor Outcome**
Poor outcome was defined as modified Rankin Scale 4–6 at 3 months. (A) Relative hematoma expansion. (B) Absolute hematoma expansion.

See this image and copyright information in PMC

References

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Association Between Hematoma Expansion Severity and Outcome and Its Interaction With Baseline Intracerebral Hemorrhage Volume

Affiliations

Association Between Hematoma Expansion Severity and Outcome and Its Interaction With Baseline Intracerebral Hemorrhage Volume

Authors

Affiliations

Abstract

Conflict of interest statement

Figures

References

MeSH terms

LinkOut - more resources

Full Text Sources

Medical