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Diffusion weighted imaging reversibility in the brainstem following successful recanalization of acute basilar artery occlusion
  1. Albert J Yoo1,2,
  2. Reza Hakimelahi1,
  3. Natalia S Rost3,
  4. Pamela W Schaefer1,
  5. Joshua A Hirsch2,
  6. R Gilberto González1,
  7. James D Rabinov2
  1. 1Department of Neuroradiology, Massachusetts General Hospital, Boston, Massachusetts, USA
  2. 2Department of Interventional Neuroradiology, Massachusetts General Hospital, Boston, Massachusetts, USA
  3. 3Department of Neurology, Massachusetts General Hospital, Boston, Massachusetts, USA
  1. Correspondence to Dr A J Yoo, Department of Neuroradiology and Interventional Neuroradiology, Massachusetts General Hospital, 55 Fruit Street, Gray 241, Boston, MA 02114, USA;ajyoo{at}partners.org

Abstract

Acute basilar artery occlusion (ABAO) is a devastating disease that can produce significant brainstem injury. Pretreatment diffusion weighted imaging (DWI) demonstrating extensive brainstem involvement has been shown to predict a poor outcome regardless of reperfusion. This case report describes a patient presenting with coma secondary to ABAO. MRI at presentation demonstrated significant DWI abnormality in the majority of the bilateral pons. The basilar artery was endovascularly recanalized 8 h after stroke onset, and the patient had a marked clinical recovery with no deficit at 3 months. Follow-up imaging revealed significant reversal of the pontine lesion. This finding of brainstem DWI reversibility cautions against the use of DWI to select ABAO patients for intra-arterial stroke therapy. The degree of apparent diffusion coefficient reduction on pretreatment MRI may not adequately identify which DWI abnormal brainstem tissue is potentially reversible.

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Introduction

Acute basilar artery occlusion (ABAO) is a devastating condition often resulting in disability or death. Reperfusion alone is not sufficient for a good outcome as only half of patients who recanalize achieve independence.1 Evidence of extensive brainstem ischemia on pretreatment imaging is strongly associated with poor outcome, regardless of reperfusion.2 3 In one study of 29 ABAO patients, the extent of acute brainstem diffusion weighted imaging (DWI) abnormality was the only independent predictor of functional outcome.3 However, the use of DWI to exclude ABAO patients from reperfusion therapy is limited by potential DWI reversal (tissue with restricted diffusion that appears normal on follow-up imaging). This issue is particularly relevant for neurointerventionalists, as there are only two previously reported cases of brainstem DWI reversal, both following intra-arterial reperfusion therapy.4 5 This case report adds to the current literature by discussing the imaging characteristics associated with this phenomenon.

Case report

The patient, a 67-year-old woman, was last seen normal at 10:30 h when she became unresponsive at work. At the outside hospital, she had jerking movements, right hemiplegia and right gaze deviation, and was intubated for airway protection. Outside hospital head CT scan was negative but no intravenous tissue plasminogen activator was administered due to presumed seizure. At our hospital, she remained unresponsive, with bilaterally flaccid upper extremity tone and bilateral lower extremity hypertonia (National Institutes of Health Stroke Scale score=31). CT angiography demonstrated mid-basilar artery occlusion, with a second atherosclerotic occlusion of the proximal cervical left vertebral artery (VA). MRI revealed restricted diffusion in the majority of the bilateral mid-pons (figure 1).

Figure 1

Pretreatment diffusion weighted (top) and apparent diffusion coefficient (middle) images demonstrate restricted diffusion in the majority of the bilateral pons. T2 weighted imaging (bottom) at 4 months after the stroke confirms a residual left pontine infarct with reversal in the right pons.

After family discussion, the patient was taken for intra-arterial reperfusion therapy. The femoral artery was punctured at 17:25 h. Angiography demonstrated a stump occlusion at the left VA origin with collateral reconstitution in the neck. Because the right VA was hypoplastic, the guide catheter was positioned distal to the left VA occlusion where angiography confirmed mid-basilar artery occlusion (figure 2). Local fibrinolysis was performed with 150 000 units of urokinase, resulting in recanalization at 8 h after stroke onset (figure 2). Cervical angiography revealed recanalization of the left VA occlusion, with a moderate–severe stenosis at the left VA origin which was not treated. The patient was started on intravenous heparin. Afterwards, her alertness improved, with recovery of her right lower extremity strength. She had a tracheostomy and gastric feeding tube placed. Because she was on aspirin when she had her stroke, she was started on warfarin and was discharged to a rehabilitation facility.

Figure 2

Mid-basilar artery occlusion (A) was successfully recanalized with residual clot in the left superior cerebellar and posterior cerebral arteries (B).

Three months later, the patient demonstrated a remarkable recovery with full strength in all extremities, and intact language and cognition (National Institutes of Health Stroke Scale score=0, modified Rankin scale score=0). MRI demonstrated a left pontine infarct with DWI normalization in the right pons (figure 1). Subsequent analysis revealed that the pretreatment pontine DWI lesion volume was 3.7 cm3 and the final pontine infarct volume was 1.1 cm3. The mean pretreatment apparent diffusion coefficient (ADC) values in the regions of the pons that remained infarcted, that went on to normalize and that was unaffected, were 408×10−6, 456×10−6 and 768×10−6 mm2/s, respectively.

Discussion

This case report illustrates partial but significant reversal of brainstem DWI abnormality following endovascular recanalization of ABAO. This finding was accompanied by a dramatic clinical recovery.

Recent work has demonstrated that the extent of brainstem ischemia on pretreatment CT angiography source images or DWI is the strongest predictor of clinical outcome, regardless of reperfusion.2 3 This association reflects the vital functions subserved by the brainstem. However, using DWI to exclude ABAO patients from treatment based on extensive brainstem injury cannot be recommended because of the potential for DWI reversal. This is especially relevant for neurointerventionalists as all three reported cases of brainstem DWI reversal occurred after successful intra-arterial reperfusion therapy.

Ischemic lesions on DWI are thought to represent the best estimate of the infarct core but several case series have reported partial normalization of DWI abnormalities in anterior circulation strokes6–9 with rates ranging from 19% to 44%. Reperfusion appears to be a prerequisite for this phenomenon.8 9 Other predictors include earlier time to imaging and smaller ADC reductions.8 Yet, the clinical significance of DWI reversal remains unclear. It has not been associated with improved clinical outcomes although there was a trend in one study.8 Furthermore, the mean volume of tissue reversal is relatively small (7.6–16 cm3).7–9 While such small volumes may translate to clinical improvement, it is more likely that any benefit associated with DWI reversal in the anterior circulation is related to the effects of accompanying tissue reperfusion, notably penumbral salvage.

On the other hand, small volumes of DWI reversal may have an important clinical effect in the brainstem where eloquent structures are tightly packed together. In this and a previous case report,4 two ABAO patients presented with coma, underwent endovascular reperfusion and had marked clinical recovery. Volumes of DWI reversal were only 3.8 cm3 in the previous report and 2.6 cm3 in the present one. However, both volumes encompassed the pons.

In this case, the ratio of pretreatment ADC values in pontine tissue with DWI reversal and unaffected pons was 0.59. This value is within the previously reported range10 for DWI reversibility in the white matter (0.45–0.85), which comprises the majority of the brainstem. (The reported range for gray matter is 0.72–0.79.) There was only a small difference (∼10%) in mean ADC values in brainstem tissue that normalized versus tissue that did not, which is consistent with previous reports demonstrating a significant overlap in ADC values between these two regions.6 8

The DWI sequence is designed to measure signal loss related to the diffusion of water. However, it remains unclear what aspect of cellular dysfunction results in decreased diffusivity. Proposed causes include failure of ATP pump function, fluid shifts into the intracellular space, increased intracellular viscosity and loss of cytoplasmic streaming.10 Elucidating the in vivo mechanism of restricted diffusion may help to explain the phenomenon of diffusion normalization.

It is important to note the disparity between the final infarct and the symmetric clinical improvement. This highlights the importance of infarct location even within the brainstem. Nevertheless, it is somewhat surprising that given the location of the infarct in the left paramedian basis pontis that there was no arm weakness or dysarthria. The sparing of the pontine tegmentum explains the absence of impaired consciousness, which usually results from bilateral tegmental involvement.11

Conclusion

ABAO is a devastating disease that can result in extensive brainstem injury. Normalization of DWI abnormalities can occur in the brainstem following successful endovascular treatment of ABAO, and can be associated with dramatic clinical improvement. Future studies are needed to assess the frequency of this phenomenon, its clinical significance and its predictors.

Key messages

  • Acute basilar artery occlusion is a devastating disease which can be successfully treated with intra-arterial revascularization therapy.

  • Extensive brainstem injury on pretreatment DWI has been shown to be a strong predictor of poor outcome, despite subsequent recanalization.

  • This study demonstrates that DWI abnormal brainstem tissue can undergo diffusion normalization following successful treatment of basilar artery occlusion, and this may be associated with good outcome.

  • Baseline imaging characteristics of brainstem tissue that undergoes diffusion reversal are similar to DWI abnormal tissue that sustains permanent injury.

References

Footnotes

  • Funding AJY was the 2007 recipient of the Neuroradiology Education and Research Foundation/Boston Scientific Fellowship in Cerebrovascular Disease Research.

  • Competing interests JAH is a consultant and shareholder in Intratech Medical.

  • Patient consent Obtained.

  • Ethics approval This study was approved by the institutional review board of the Partners Human Research Office.

  • Provenance and peer review Not commissioned; externally peer reviewed.