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Temporal changes in perihematomal apparent diffusion coefficient values during the transition from acute to subacute phases in patients with spontaneous intracerebral hemorrhage

  • Diagnostic Neuroradiology
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Abstract

Introduction

Diffusion-weighted imaging (DWI) studies focusing on apparent diffusion coefficient (ADC) abnormalities have provided conflicting results about the nature and fate of perihematomal edema.

Methods

We investigated 35 patients with supratentorial spontaneous intracerebral hemorrhage (SICH) by using DWI scanning obtained at 48 h and 7 days after symptom onset. Regional ADC (rADC) values were measured in three manually outlined regions of interest: (1) the perihematomal hyperintense area, (2) 1 cm of normal appearing brain tissue surrounding the perilesional hyperintense rim, and (3) a mirror area, including the clot and the perihematomal region, located in the contralateral hemisphere.

Results

rADC mean levels were lower at 7 days than at 48 h in each ROI (p < 0.00001), showing a progressive normalization of initial vasogenic values. Perihematomal vasogenic rADC values were more frequent (p < 0.00001) at 48 h than at 7 days, whereas perihematomal cytotoxic and normal rADC levels were more represented (p < 0.02 and p < 0.001, respectively) at 7 days than at 48 h. A neurological worsening was more frequent (p < 0.02) in patients with than in those without perihematomal cytotoxic rADC values at 7 days.

Conclusion

Our findings suggest that the transition from acute to subacute phases after SICH is characterized by a progressive resolution of perihematomal vasogenic edema associated with an increase in cytotoxic ADC values. In the subset of patients with perihematomal cytotoxic rADC levels in subacute stage after bleeding, irreversible damage development seems to be related to poor clinical outcome.

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References

  1. Qureshi AI, Mendelow AD, Hanley DF (2009) Intracerebral haemorrhage. Lancet 373:1643–1644

    Article  Google Scholar 

  2. Xi G, Keep RF, Hoff JT (2006) Mechanisms of brain injury after intracerebral haemorrhage. Lancet Neurol 5:53–63

    Article  PubMed  Google Scholar 

  3. Leira R, Dávalos A, Silva Y, Gil-Peralta A, Tejada J, Garcia M, Castillo J, for the Stroke Project, Cerebrovascular Diseases Group of the Spanish Neurological Society (2004) Early neurologic deterioration in intracerebral hemorrhage. Predictors and associated factors. Neurology 63:461–467

    Article  PubMed  CAS  Google Scholar 

  4. Davis SM, Broderick J, Hennerici M, Brun NC, Diringer MN, Mayer SA, Begtrup K, Steiner T, for the Recombinant Activated Factor VII Intracerebral Hemorrhage Trial Investigation (2006) Hematoma growth is a determinant of mortality and poor outcome after intracerebral hemorrhage. Neurology 66:1175–1181

    Article  PubMed  CAS  Google Scholar 

  5. Dowlatshahi D, Demchuck AM, Flaherty ML, Ali M, Lyden PL, Smith EE, on behalf of the VISTA Collaboration (2011) Defining hematoma expansion in intracerebral hemorrhage. Relationship with patient outcomes. Neurology 76:1238–1244

    Article  PubMed  CAS  Google Scholar 

  6. Gebel JM, Jauch EC, Brott TG, Khoury J, Sauerbeck L, Salisbury S, Spilker J, Tomsick TA, Duldner J, Broderick JP (2002) Relative edema volume is a predictor of outcome in patients with hyperacute spontaneous intracerebral hemorrhage. Stroke 33:2636–2641

    Article  PubMed  Google Scholar 

  7. Venkatasubramanian C, Mlynash M, Finley-Caulfield A, Eyngorn I, Kalimuthu R, Snider RW, Wijman CA (2011) Natural history of perihematomal edema after intracerebral haemorrhage measured by serial magnetic resonance imaging. Stroke 42:73–80

    Article  PubMed  Google Scholar 

  8. Staykov D, Wagner I, Volbers B, Hauer E-V, Doerfler A, Schwab S, Bardutzky J (2011) Natural course of perihemorrhagic edema after intracerebral haemorrhage. Stroke 42:2625–2629

    Article  PubMed  Google Scholar 

  9. Arima H, Wang JG, Huang Y, Heeley E, Skulina C, Parsons MW, Peng B, Li Q, Su S, Tao QL, Li YC, Jiang JD, Tai LW, Zhang JL, Xu E, Cheng Y, Morgenstern LB (2009) Anderson CS for the INTERACT Investigators. Neurology 73:1963–1968

    Article  PubMed  CAS  Google Scholar 

  10. Huisman TAG (2003) Diffusion-weighted imaging: basic concepts and application in cerebral stroke and head trauma. Eur Radiol 13:2283–2297

    Article  PubMed  Google Scholar 

  11. Orakcioglu B, Fierbach JB, Steiner T, Kollmar R, Jüttler E, Becker K, Schwab S, Heiland S, Meyding-Lamadé UK, Schellinger PD (2005) Evolution of early perihemorrhagic changes—ischemia vs. edema: an MRI study in rats. Exp Neurol 193:369–376

    Article  PubMed  CAS  Google Scholar 

  12. Orakcioglu B, Becker K, Sakowitz O, Herweh C, Köhrmann M, Huttner HB, Steiner T, Unterberg A, Schellinger PD (2008) MRI of the perihemorrhagic zone in a rat ICH model: effect of hematoma evacuation. Neurocrit Care 8:448–455

    Article  PubMed  Google Scholar 

  13. Kidwell CS, Saver JL, Mattiello J, Warach S, Liebeskind DS, Starkman S, Vespa PM, Villablanca JP, Martin NA, Frazee J, Alger JR (2001) Diffusion–perfusion MR evaluation of perihematomal injury in hyperacute intracerebral hemorrhage. Neurology 57:1611–1617

    Article  PubMed  CAS  Google Scholar 

  14. Schellinger PD, Fiebach JB, Hoffmann K, Becker K, Orakcioglu B, Kollmar R, Jüttler E, Schramm P, Schwab S, Sartor K, Hacke W (2003) Stroke MRI in intracerebral hemorrhage. Is there a perihemorrhagic penumbra? Stroke 34:1674–1680

    Article  PubMed  Google Scholar 

  15. Morita N, Harada M, Yoneda K, Nishitani H, Uno M (2002) A characteristic feature of acute haematomas in the brain on echo-planar diffusion-weighted imaging. Neuroradiology 44:907–911

    Article  PubMed  CAS  Google Scholar 

  16. Carhuapoma JR, Wang P, Beauchamp NJ, Keyl PM, Hanley DF, Barker PB (2000) Diffusion-weighted MRI and proton MR spectroscopy imaging in the study of secondary neuronal injury after intracerebral hemorrhage. Stroke 31:726–732

    Article  PubMed  CAS  Google Scholar 

  17. Carhuapoma JR, Barker PB, Hanley DF, Wang P, Beauchamp NJ (2002) Human brain hemorrhage: quantification of perihematoma edema by use of diffusion-weighted MR imaging. AJNR Am J Neuroradiol 23:1322–1326

    PubMed  Google Scholar 

  18. Butcher KS, Baird T, MacGregor L, Desmond P, Tress B, Davis S (2004) Perihematomal edema in primary intracerebral hemorrhage is plasma derived. Stroke 35:1879–1885

    Article  PubMed  Google Scholar 

  19. Forbes KP, Pipe JG, Heiserman JE (2003) Diffusion-weighted imaging provides support for secondary neuronal damage from intraparenchymal hematoma. Neuroradiology 45:363–367

    Article  PubMed  CAS  Google Scholar 

  20. Kamal AK, Dyke JP, Katz JM, Liberato B, Filippi CG, Zimmerman RD, Uluğ AM (2003) Temporal evolution of diffusion after spontaneous supratentorial intracranial hemorrhage. AJNR Am J Neuroradiol 24:895–901

    PubMed  Google Scholar 

  21. Fainardi E, Borrelli M, Saletti A, Schivalocchi R, Russo M, Azzini C, Cavallo M, Ceruti S, Tamarozzi R, Chieregato A (2006) Evaluation of perihematomal regional apparent diffusion coefficient abnormalities by diffusion-weighted imaging. Acta Neurochir 96(Suppl):81–84

    Article  CAS  Google Scholar 

  22. Olivot J-M, Mlynash M, Klienman JT, Straka M, Venkatasubramanian C, Bammer R, Moseley ME, Albers GW, Wijman AC, for the DASH Investigators (2010) MRI profile of the perihematomal region in acute intracerebral hemorrhage. Stroke 41:2681–2683

    Article  PubMed  Google Scholar 

  23. Chieregato A, Fainardi E (2008) Potential role of surgery in traumatic focal brain lesions as revealed by functional imaging. Intensive Care Med 34:2125–2126

    Article  PubMed  Google Scholar 

  24. Morgenstern JB, Hemphill JC III, Anderson C, Becker K, Broderick JP, Connolly ES Jr, Greenberg SM, Huang JN, Macdonald RL, Messé SR, Mitchell PH, Selim M, Tamargo RJ, American Heart Association Stroke Council and Council on Cardiovascular Nursing (2010) Guidelines for the management of spontaneous intracerebral hemorrhage: a guideline for healthcare professionals from the American heart Association/American Stroke Association. Stroke 41:2108–2129

    Article  PubMed  Google Scholar 

  25. Brott T, Adams HP, Olinger CP, Marler JR, Barsan WG, Biller J, Spilker J, Holleran R, Eberle R, Hertzberg V, Rorick M, Moomaw CJ, Walker M (1989) Measurements of acute cerebral infarction: a clinical examination scale. Stroke 20:864–870

    Article  PubMed  CAS  Google Scholar 

  26. The National Institute of Neurological Disorders and Stroke rt-PA Study Group (1995) Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 333:1581–1587

    Article  Google Scholar 

  27. Ulug AZ, Beauchamp N, Bryan RN, van Zijl PCM (1997) Absolute quantitation of diffusion constants in human stroke. Stroke 28:483–490

    Article  PubMed  CAS  Google Scholar 

  28. Alemany Ripoll M, Stenborg A, Sonninen P, Terent A, Raininko R (2004) Detection and appearance of intraparenchymal haematomas of the brain at 1.5T with spin-echo, FLAIR and GE sequences: poor relationship to the age of the haematoma. Neuroradiology 46:435–443

    Article  PubMed  CAS  Google Scholar 

  29. Volbers B, Staykov D, Wagner I, Dörfler A, Saake M, Schwab S, Bardutzky J (2011) Semi-automatic volumetric assessment of perihemorrhagic edema with computed tomography. Eur J Neurol 18:1323–1328

    Article  PubMed  Google Scholar 

  30. Burgess RE, Warach S, Schaewe TJ, Copenhaver BR, Alger JR, Vespa P, Martin N, Saver JL, Chelsea S, Kidwell CS (2008) Development and validation of a simple conversion model for comparison of intracerebral hemorrhage volumes measured on CT and gradient recalled echo MRI. Stroke 39:2017–2020

    Article  PubMed  Google Scholar 

  31. Brott T, Broderick J, Kothari R, Barsan W, Tomsick T, Sauerbeck L, Spilker J, Duldner J, Khoury J (1997) Early hemorrhage growth in patients with intracerebral hemorrhage. Stroke 28:1–5

    Article  PubMed  CAS  Google Scholar 

  32. Maldjian JA, Listerud J, Moonis G, Siddiqi F (2001) Computing diffusion rates in T2-dark hematomas and areas of low T2 signal. AJNR Am J Neuroradiol 22:112–118

    PubMed  CAS  Google Scholar 

  33. Lou M, Lieb K, Selim M (2009) The relationship between hematoma iron content and perihematomal edema: an MRI study. Cerebrovasc Dis 27:266–271

    Article  PubMed  CAS  Google Scholar 

  34. Khatri IA, Verma N, Alkawi A, Janjua N, Kirmani JF (2009) Cerebral vasospasm in intracerebral hemorrhage—case report. J Vasc Interv Neurol 2:139–141

    PubMed  Google Scholar 

  35. Wardlaw JM (2010) Blood–brain barrier and cerebral small vessel disease. J Neurol Sci 299:66–71

    Article  PubMed  CAS  Google Scholar 

  36. Kidwell CS, Burgess R, Menon R, Warach S, Latour LL (2011) Hyperacute injury marker (HARM) in primary hemorrhage. A distinct form of CNS barrier disruption. Neurology 77:1725–1728

    Article  PubMed  CAS  Google Scholar 

  37. Latour LL, Kang D-W, Ezzedine MA, Chalela JA, Warach S (2004) Early blood–brain barrier disruption in human focal brain ischemia. Ann Neurol 56:468–477

    Article  PubMed  Google Scholar 

  38. Lou M, Al-Hazzani A, Goddeau RP, Novak V, Selim M (2010) Relationship between white-matter hyperintensities and hematoma volume and growth in patients with intracerebral hemorrhage. Stroke 41:34–40

    Article  PubMed  Google Scholar 

  39. Lee S-H, Kim BJ, Ryu W-S, Kim CK, Kim N, Park B-J, Yoon B-W (2010) White matter lesions and poor outcome after intracerebral hemorrhage. A nationwide cohort study. Neurology 74:1502–1510

    Article  PubMed  Google Scholar 

  40. Prabhakaran S, Gupta R, Ouyang B, John S, Temes RE, Mohammad Y, Lee VH, Bleck TP (2010) Acute brain infarcts after spontaneous intracerebral hemorrhage. A diffusion-weighted imaging study. Stroke 41:89–94

    Article  PubMed  Google Scholar 

  41. Gregorie SM, Charidimou A, Gadapa N, Dolan E, Antoun N, Peeters A, Vandermeeren Y, Laloux P, Baron J-C, Jäger HR, Werring DJ (2011) Acute ischaemic brain lesions in intracerebral haemorrhage: multicentre cross-sectional magnetic resonance imaging study. Brain 134:2376–2386

    Article  Google Scholar 

  42. Steiner T, Bösel J (2010) Options to restrict hematoma expansion after spontaneous intracerebral hemorrhage. Stroke 41:402–409

    Article  PubMed  Google Scholar 

  43. Sasaki M, Yamada K, Watanabe Y, Matsui M, Ida M, Fujiwara S, Shibata E, for the Acute Stroke IMAGING Standardization Group-Japan (ASIST-Japan) Investigators (2008) Variability in absolute apparent diffusion coefficient values across different platforms may be substantial: a multivendor multi-institutional comparison study. Radiology 249:624–630

    Article  PubMed  Google Scholar 

  44. Helenius J, Soinne L, Salonen O, Kaste M, Tatlisumak T (2002) Leukoaraiosis, ischemic stroke, and normal white matter on diffusion-weighted MRI. Stroke 33:45–50

    Article  PubMed  Google Scholar 

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Acknowledgments

The authors thank Dr. Elizabeth Jenkins for helpful corrections to the manuscript.

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We declare that we have no conflict of interest.

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Correspondence to Enrico Fainardi.

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Fainardi, E., Borrelli, M., Saletti, A. et al. Temporal changes in perihematomal apparent diffusion coefficient values during the transition from acute to subacute phases in patients with spontaneous intracerebral hemorrhage. Neuroradiology 55, 145–156 (2013). https://doi.org/10.1007/s00234-012-1093-x

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  • DOI: https://doi.org/10.1007/s00234-012-1093-x

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