Elsevier

World Neurosurgery

Volume 83, Issue 6, June 2015, Pages 1006-1014
World Neurosurgery

Original Article
Quantification of Corticospinal Tracts with Diffusion Tensor Imaging in Brainstem Surgery: Prognostic Value in 14 Consecutive Cases at 3T Magnetic Resonance Imaging

https://doi.org/10.1016/j.wneu.2015.01.045Get rights and content

Objective

In this study, we investigated the potential prognostic role of morphologic and quantitative diffusion tensor imaging (DTI) in patients with brainstem cavernoma (BSC) in terms of postoperative outcome.

Methods

In this retrospective study of 14 brainstem cavernoma patients, we analyzed pre- and postoperative DTI data. White matter tractography of corticospinal tracts (CSTs) was performed with the Fiber Assignment by Continuous Tracking algorithm, and morphologic characteristics of CSTs were compared with clinically assessed motor strength. Fractional anisotropy (FA) and apparent diffusion coefficient (ADC) were measured in ipsi- and contralesional regions of interest at the lesion level, as well as levels caudal and rostral to the lesion. Correlation analysis was performed between lateral index (LI) of ipsi-/contralateral FA and ADC values and patients' motor function.

Results

Preoperatively, normal morphologic features of CSTs corresponded to normal motor function in 4 patients. The other 10 morphologically abnormal preoperative CSTs didn't show corresponding motor impairment either in pre- or postoperative follow-up period. The sensitivity, specificity, positive predictive, and negative predictive values of white matter tractographic morphology on preoperative motor function were 100%, 57.1%, 70%, and 100%, respectively. The corresponding values on follow-up motor function were 100%, 33.3%, 20%, and 100%, respectively. The mean FA at lesion level was significantly lower than the corresponding FA at the contralateral hemisphere (P = 0.009). In areas caudal to the lesion the same trend yet without statistic significance was observed (P = 0.23). There was no significant laterality difference of mean FAs rostral to the level of the lesion. No correlation in LI of FA or ADC in the 3 anatomic levels with simultaneous and long-term follow up motor function was observed. Restoration of the morphology of the affected CST postoperatively was associated with a trend for decreasing ADC compared with the preoperative measurements.

Conclusion

Intact CST morphology in DTI predicts a favorable postoperative outcome in patients with BSC. Interrupted CSTs and decreased FA values correlate well within BSC lesion level; nevertheless, morphologic characteristics and diffusion parameter changes at lesion level cannot predict poor prognosis. Caudal and rostral diffusion parameters can provide more information of the integrity of CSTs compared with morphologic study alone.

Introduction

In recent years, the incidence of brain cavernomas has increased as the result of advances in neuroimaging, particularly the widespread use of magnetic resonance imaging (MRI) in clinical practice. The prevalence of intracranial cavernomas ranges from 0.4% to 0.9% 8, 28, with the ones being localized in the brainstem representing 8%–22% (11). This subgroup of cavernomas has a substantially greater tendency for bleeding (up to 30%) (25), which is more likely to result in severe neurologic deficits 7, 11, 25 and moreover has a greater incidence of recurrent hemorrhage than those in other locations 26, 34. Surgical extirpation is the major treatment option for the symptomatic brainstem cavernomas (BSCs). Because of their location deep within a relatively small anatomic region, highly compact in functionally important white matter tracts and grey matter nuclei, BSCs to date remain a major challenge for neurosurgeons. They also represent a challenge for a functionally relevant neuroradiologic description because of the poor differentiation of individual anatomical structures on conventional MRI.

Diffusion tensor imaging (DTI) is a recently introduced technique that allows evaluation of white matter integrity by virtue of its ability to visualize water diffusion characteristics. White matter tractography (WMT), also known as “fiber tracking,” allows 3-dimensional visualization of white matter tracts and accurate description of their architecture and integrity in the brainstem 2, 12, 21. The validity and reliability of WMT via the use of DTI for brainstem lesions in preoperative planning have been well demonstrated in previous studies 6, 22. Recent studies in patients with brain tumors have used quantitative DTI parameters, namely apparent diffusion coefficient (ADC) and fractional anisotropy (FA), for histologic prediction of the tumor 15, 19, 29 and to characterize the effects of the tumor on the surrounding white matter tracts 5, 10. On the basis of these studies, several institutions have adopted DTI as an increasingly important component of preoperative planning in patients with supratentorial tumors (35) and brainstem lesions 5, 31, 32.

Currently, there are no clinical or imaging findings that can reliably predict postoperative motor function in patients with BSCs. Our hypothesis is that the structural morphology and quantitative measures of DTI in these patients might provide prospectively prediction of postoperative clinical findings and outcome and, thus, hold certain prognostic value for more informed therapy decision making. To test this hypothesis, we investigated the prognostic value of morphologic and quantitative imaging parameters generated from WMT of corticospinal tract (CST) using pre- and postoperative DTI in 14 patients with BSCs.

Section snippets

Materials and Methods

DTI data were analyzed in a retrospective study of 14 patients with BSC, which were operated between January of 2008 and June of 2010 at the department of neurosurgery. Each diagnosis was confirmed by histology. Patients' details are listed in Table 1. The mean age of the patients was 36 years (range, 6–63 years). Most of the lesions located in the pons (10/14, 71.4%); 1 lesion in the mesencephalon (7.1%); 2 lesions in the medulla oblongata (14.2%); and 1 lesion involved both pons and

Results

All patients showed either improvement of their symptoms or had stable neurological status without any additional complications. The 14 patients' contralateral motor functions at 3 time points are shown in Table 1.

Discussion

DTI-WMT is currently the only noninvasive method that can visualize the human white matter tracts in vivo. This technique has a proven value for planning a safer surgical approach but also a prospective potential for predicting postoperative motor function. To date, this has been reported mostly in supratentorial tumor surgery 18, 36. Previous studies have reported that for supratentorial lesions, preoperative CST involvement may be a predictor of motor deficit and that postoperative

Conclusions

Normal CST morphology generated from WMT using DTI predicts a favorable postoperative outcome in patients with BSC. Interrupted CSTs and decreased FA values correlate well within BSC lesion level. However, morphologic characteristics and diffusion parameter changes at lesion level cannot predict poor prognosis. Caudal and rostral diffusion parameters can provide more information of the integrity of CSTs compared with morphologic study alone.

Acknowledgments

The authors are very grateful to all patients for participating in this study and thank Dr. Uzeyir Ahmadli for neuroradiological consultation in fiber tracking.

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    Conflict of interest statement: The authors declare that the article content was composed in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

    Yuqiang Yao and Nils H. Ulrich are co–first authors.

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