Elsevier

World Neurosurgery

Volume 114, June 2018, Pages e624-e630
World Neurosurgery

Original Article
Significant Injury of the Mammillothalamic Tract without Injury of the Corticospinal Tract After Aneurysmal Subarachnoid Hemorrhage: A Retrospective Diffusion Tensor Imaging Study

https://doi.org/10.1016/j.wneu.2018.03.042Get rights and content

Highlights

  • Patients with good outcomes after aSAH appeared to suffer an injury of the MTT.

  • This injury showed correlation with cognitive dysfunction.

  • Patients with aSAH with good outcomes may not show motor deficits.

  • However, they still may complain about long-term cognitive dysfunction.

Objective

Little is known about the pathophysiologic mechanisms of white matter injury after aneurysmal subarachnoid hemorrhage (aSAH). The purpose of this study is to investigate whether the mammillothalamic tract (MTT) or corticospinal tract (CST) is more affected by aSAH in the same patients with good outcome (Grade 5 on Glasgow Outcome Scale at 3 months) using diffusion tensor imaging (DTI).

Methods

Between June 2013 and September 2016, 21 patients with aSAH with good outcome and 21 sex- and age-matched normal healthy control participants were recruited. DTI was obtained at 8.92 ± 2.4 weeks after onset. Moreover, reconstruction of the CST and the MTT was completed with DTI-studio software. Apparent diffusion coefficient (ADC) and fractional anisotropy (FA) values were measured. In addition, the motricity index and Mini-Mental State Examination scores were obtained.

Results

There was no statistically significant difference detected in the ADC and FA values of the CST between the patient and control groups (P > 0.05). On the contrary, there was a statistically significant difference in ADC and FA values of the MTT between the patient and control groups (P < 0.05). In addition, in the patient group, no correlation (P > 0.05) was observed between motricity index scores and DTI parameters (ADC and FA), whereas the Mini-Mental State Examination showed a positive correlation with FA (r = 0.591, P = 0.029) without correlation to ADC (r = 0.142, P = 0.628).

Conclusions

Patients with good outcomes (Grade 5 on Glasgow Outcome Scale at 3 months) after aSAH appeared to suffer an injury of the MTT without an associated injury of the CST compared with the control group. This injury showed a correlation with cognitive dysfunction.

Introduction

Subarachnoid hemorrhage (SAH) is bleeding into the subarachnoid space. It comprises 5% of all patients with stroke.1, 2, 3 The average mortality rate after SAH is 51%.3, 4 Most patients die within 2 weeks and around 25% within first 24 hours after SAH. In addition, life-long care is needed for approximately one-third of survivors.3, 4

Various neurologic complications occur after SAH, including motor weakness, memory impairment, cranial nerve dysfunction, and somatosensory deficits.2, 3, 4, 5 Motor weakness has been reported to range from 14% to 29%.1, 5, 6, 7 In addition, memory impairment is another very common sequela after SAH.2, 5 Various pathophysiologic mechanisms have been suggested: primary brain injury by SAH, vasospasm, compression by an aneurysm, or insufficient blood perfusion of paracentral areas. Furthermore, several studies have reported on the possible mechanisms of neural injury after SAH by using diffusion tensor imaging (DTI).2, 5, 7, 8 However, the exact pathophysiologic mechanisms have not been clearly illustrated so far.1, 5, 7

DTI is a newly introduced technique that evaluates the integrity of the white matter tracts that cannot be assessed by conventional magnetic resonance imaging by virtue of its capability to visualize water diffusion characteristics.1, 4, 7, 9, 10, 11, 12, 13, 14 In addition, it can detect subtle but clinically meaningful changes after SAH.1, 2, 3, 7, 11 Diffusion tensor tractography, which is derived from DTI, allows for 3-dimensional visualization of the integrity and architecture of the white matter tracts.1, 2, 4, 8, 9, 10, 11, 12, 13, 14, 15, 16

As for DTI parameters, the fractional anisotropy (FA) value describes the degree of water diffusion directionality and has a range of 1 (totally anisotropic diffusion) to 0 (totally isotropic diffusion). Moreover, it demonstrates the integrity and the degree of directionality of white matter microstructures such as microtubules, myelin, and axons. Thus, a reduction in the FA value indicates a neural tract injury.2, 3, 4, 6, 7, 8, 9, 13, 15, 16, 17 The apparent diffusion coefficient value describes the magnitude of water diffusion that can increase under conditions of cytotoxic or vasogenic edema or cellular debris accumulation after axonal injury.3, 13, 15, 17

The corticospinal tract (CST), which starts at the cortex and terminates on motor neurons in the spinal cord, is responsible for controlling movements of the limbs.4, 7, 9, 10, 11, 12, 13, 14, 15, 18 The mammillothalamic tract (MTT), which is involved in episodic memory, is a part of the Papez circuit that connects between the anterior thalamus and the mammillary body.2, 8, 16 The motricity index (MI) is a valid and reliable test to assess motor impairment after stroke.19 Furthermore, in screening for cognitive dysfunction, the Mini-Mental State Examination (MMSE) is a widely used tool.2, 20

The purpose of this study was to examine which white matter tract (CST or MTT) is affected more by aSAH in the same patients with good outcome (Grade 5 on Glasgow Outcome Scale [GOS] at 3 months) using DTI. It was expected that, since most patients with aSAH with good outcome complain about long-term cognitive dysfunction without experiencing motor deficits, the MTT would be more affected by aSAH compared with CST. We believe that the findings of this retrospective study can bring the researchers one step closer to understanding the pathophysiologic mechanism of aSAH and provide a better understanding to develop a more efficient rehabilitation plan of care for patients with good outcome after aSAH.

Section snippets

Subjects

Between June 2013 and September 2016, 21 patients (Grade 5 on GOS at 3 months) with aSAH with good outcome (female: 17, male: 4, mean age: 54.21 ± 6.4 years, range: 45∼66 years) and 21 sex- and age-matched normal healthy control participants (female: 17, male: 4, mean age: 53.00 ± 6.2 years, range: 45∼65 years) with no previous history of stroke (whether ischemic or hemorrhagic), hydrocephalus, intracerebral hemorrhage, intraventricular hemorrhage, brain injury, brain surgery, mental diseases,

Results

Twenty-one patients with good outcome (Grade 5 on GOS at 3 months) with aSAH (female: 17, male: 4, mean age: 54.21 ± 6.4 years, range: 45∼66 years) and 21 sex- and age-matched normal healthy control participants (female: 17, male: 4, mean age: 53.00 ± 6.2 years, range: 45∼65 years) with no previous history of stroke (whether ischemic or hemorrhagic), hydrocephalus, intracerebral hemorrhage, intraventricular hemorrhage, brain injury, brain surgery, mental diseases, or other neurologic disease

Discussion

In this retrospective study, using DTI, we found a significant injury of the MTT without associated injury of the CST after aSAH. Many studies have tried to explain the pathophysiologic mechanism of neural injury after SAH.1, 2, 3, 5, 6, 7, 8, 13, 16, 18, 26, 27 Unfortunately, the full mechanism has not been explained completely. In addition, a few DTI studies have reported on the possible mechanisms of neural injury.2, 5, 7, 8

In 2014, Ma et al.6 demonstrated that the direct damage caused by

Conclusions

In summary, patients with good outcomes (Grade 5 on GOS at 3 months) after aSAH appeared to suffer an injury of the MTT without associated injury of the CST compared with the control group. This injury showed a correlation with cognitive dysfunction.

Although patients with aSAH with good outcomes may not show motor deficits, they still may experience and complain about long-term cognitive dysfunction. In addition, these patients often are neglected by physicians and not completely treated

Acknowledgments

The authors thank the Department of Neurosurgery, The First Affiliated Hospital of Chongqing Medical University, Chongqing, China. We also give a big thanks to all patients and their families for their patience and support. Finally, special thanks to the nursing staff for their help and efforts.

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    Conflict of interest statement: This work was supported by grants from the National Natural Science Foundation of China (Grant numbers 81571159 and 81671160), the National Key Clinical Specialty Construction Project of China (Grant number {2011}170), and Chongqing Key Discipline (Grant number 40010200010008).

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