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Bilateral Wallerian degeneration of the medial cerebellar peduncles after ponto-mesencephalic infarction
European Journal of Radiology 49 (2004) 198–203
Bilateral Wallerian degeneration of the medial cerebellar peduncles after ponto-mesencephalic infarction Clemens Fitzek a,b,∗ , Sabine Fitzek c,d , Peter Stoeter a b
a Institute of Neuroradiology, University of Mainz, Mainz, Germany Department of Diagnostic and Interventional Radiology, Friedrich Schiller University of Jena, Jena, Germany c Department of Neurology, University of Mainz, Mainz, Germany d Department of Neurology, Friedrich Schiller University of Jena, Jena, Germany
Received 18 February 2003; received in revised form 7 April 2003; accepted 9 April 2003
Abstract Three patients with acute large paramedian ponto-mesencephalic infarctions developed a bilateral retrograde degeneration of the medial cerebellar peduncles within 4 months after the insult. In an initial magnetic resonance imaging (MRI) within the first 2 weeks, the medial cerebellar peduncles showed normal intensities, but a control MRI after 4 months showed bright hyperintensities in the T2-TSE weighted images, and moderately increased signal intensities in echo planar imaging–diffusion weighted imaging were seen, possibly representing bilateral Wallerian degeneration of the cerebellar-pontine fibers. © 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Brain stem; MRI; Diffusion weighted imaging; Wallerian degeneration
1. Introduction
2. Patients and methods
Wallerian degeneration of the tractus pyramidalis after lesions of the motor cortex or the brainstem is well described [1–4] and independently of the kind of lesion, specific magnetic resonance imaging (MRI) signal changes develop in the corticospinal tract during the following months [5]. After peripheral and central lesions Wallerian degeneration is described such as degeneration within the optic nerves after lateral geniculate body lesion [4] or olivary degeneration after intracranial haemorrhage or trauma [6–11]. In Wallerian degeneration myelinated fibres show a loss of the cytoplasmic circumferential bands and longitudinal columns and their associated membrane pores [12]. Macrophage recruitment for myelin removal also takes place [13]. These changes of demyelination lead to signal increase in T2-weighted images (T2w), which is also measurable by diffusion weighted imaging (DWI) [14–17].
2.1. Patients
∗ Corresponding author. Tel.: +49-3641-93-5376; fax: +49-3641-93-6767. E-mail address: [email protected] (C. Fitzek).
Three patients with acute paramedian ponto-mesencephalic brainstem infarction and consequent degeneration of the medial cerebellar peduncle were included. 2.2. CT/MRI Computer tomography (CT) scan without application of contrast medium was performed immediately after admission of the patient to hospital. Up to three MRI were performed: the first MRI (MR0) in the first day after onset of symptoms or admission of the patient to hospital (echo planar imaging (EPI) DWI: TR/TE = 4000/103 ms, with separately applied diffusion-gradients in three spatial axis, b = 1164 s/mm3 , 128 matrix, 250 ms per slice, 20 slices, thickness 3 mm, 8 measurements). The slice orientation was perpendicular to the sagittal brainstem cuts. The second MRI (MR1) was performed within the first 2 weeks after the infarction (T2w-TSE: TR/TE = 3810/90 ms, 256 matrix, thickness 3 mm, T1w: TR/TE = 600/14 ms, 256 matrix, thickness 3
0720-048X/$ – see front matter © 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0720-048X(03)00132-3
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
199
Fig. 1. Fifty-nine years old female patient (patient 1) with acute ponto-mesencephalic infarction and increased signal in DWI (a) one day after onset of symptoms. At the same time no lesion of the middle cerebellar peduncle visible in T2w-TSE (b). In the control MRI after 4 months bright signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d). Delineation of the left sided paramedian infarction in control MRI in T2w-TSE (e), with a second contralateral paramedian area of increased signal not present on first examination, which possibly represents Wallerian degeneration.
200
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
mm). The control MRI (MR2) was performed 4 months later with T2w-TSE (TR/TE = 3810/90 ms, 256 matrix, thickness 3 mm). The DWI signal was regarded as hyperintense only when it was increased in all three im-
ages with direction-selective gradient application. The apparent diffusion coefficient (ADC) values were postprocessed off line and were calculated based on the Stejskal–Tanner-equation.
Fig. 2. Sixty-two years old female patient (patient 2) with acute ponto-mesencephalic infarction with increased signal in DWI (a) but normal middle cerebellar peduncles at that time (b). In control MRI after 4 months increased signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d) and sharply deliniated infarction in T2w-TSE (e).
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
201
Fig. 3. Seventy-three years old male patient (patient 3) with a well delineated mesencephalic infarction in the T2w-TSE sequence (a), but normal middle cerebellar peduncles (b). The control MRI after 4 months of symptom onset shows increased signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d).
3. Results 3.1. General characteristics There were three patients one men and two women (age 73, 62, 59 years) with acute ponto-mesencephalic paramedian brain stem infarctions. All three patients had initial symptoms of gait ataxia, dysarthria and contralateral hemiparesis with good improvement during the following 4–5 months. At the follow up only mild gait disturbance and slight hemiparesis was found.
toms indicated the acute stage of the brain stem infarction in the initially scans. In all cases, the medial cerebellar peduncles were normal. In the follow up MRI after 4 months after stroke onset, all three patients developed bright hyperintensities along both medial cerebellar peduncles in the EPI–DWI and the T2w sequences (Figs. 1–3). In two patients the ADC values were slightly decreased compared to the normal, unaffected cerebellar tracts of the inferior and superior peduncles (7.99 × 10−4 mm2 /s vs. 8.05 × 10−4 mm2 /s and 6.87 × 10−4 mm2 /s vs. 8.59 × 10−4 mm2 /s) and in one patient increased ADC values (10.67 × 10−4 mm2 /s vs. 7.39 × 10−4 mm2 /s) were measured.
3.2. MRI In the acute phase all three patients had large paramedian ponto-mesencephalic stroke lesions covering the crossing area of the medial cerebellar peduncle fibers. All three lesions showed bright signal in EPI–DWI. The signal increase in EPI–DWI together with the acute onset of symptoms and the accordance of the lesions to the clinical symp-
4. Discussion We describe three patients with first time acute brain stem stroke and corresponding large unilateral paramedian ponto-mesencephalic ischemic brain stem lesions. The majority of brain stem infarctions do not cross the midline
202
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
[18–20]. Only in few cases, especially in basilar artery thrombosis, bilateral brain stem infarctions may occur [19–21]. Brain stem infarctions, except those due to basilary thrombosis, have a good prognosis concerning the clinical outcome [22]. Wallerian degeneration does not seem to be a marker for a bad outcome in general [23], and the three patients of our study improved clinically. The middle cerebellar peduncles (brachium pontis) contain the ponto-cerebellar tract (PCT) fibers. These fibers arise from the contralateral pontine nuclei (secondary neurons) which receive collaterals from cortico-pontine tracts. The ponto-cerebellar fibers cross at an upper pontine level [24,25]. Crossed cerebellar atrophy after supratentorial lesions concerning the cortico-pontine tract is well described [26,27]. In the three patients of this series a large unilateral paramedian lesion covered the crossing area of the ponto-cerebellar fibers which become the medial cerebellar peduncle. Consequently both the fiber tracts were affected, one proximally and the other one distally to the decussatio (Fig. 4). In Wallerian degeneration the affected tracts are seen hypointense in CT [28] and show increased signal in T2w MR images and also in DWI [14–17,29] as in our three cases. Wallerian degeneration can be seen histologically a few days after the lesion [30,31]. There are case reports that DWI can show signal increase in affected areas as soon as 12 days after stroke [29]. Our patients showed remaining signal increase in DWI and T2w after 4 months after stroke onset. Water diffusion changes in Wallerian degeneration can be measured with diffusion tensor imaging, too. There seems to be a dependence on white matter architecture were diffusion anisotropy is especially reduced in regions were white matter fibers are arranged in parallel bundles [32]. Our patients showed the described high signal in DWI mainly in the pontine and proximal cerebellar portions of the middle cerebellar tract, were the fibers run predominantly parallel. The reason for the signal increase of T2w or hypodensity in CT probably is due to increased accumulation of water [28,30,31], whereas the reason for the signal increase of the
Fig. 4. Schematic drawing of the tracts (dashed lines): Cortico-pontine and cortico-spinal tracts (TP) including those from the motor cortex (MC) give collaterals to the pontine nuclei (PN). The ponto-cerebellar fibers originate from these nuclei, cross at an upper pontine level and reach the cerebellum through the middle cerebellar peduncles (MCP). A large paramedian lesion (gray area) will affect both MCPs.
DWI with partially decreased, partially elevated ADC-values remains speculative: cell swelling, demyelinisation with axonal degeneration, phagocytotic activity and water uptake are possibly involved [13–17].
5. Conclusion Large paramedian lesions which cover the crossing zone of the medial cerebellar peduncles can lead to a bilateral Wallerian degeneration of the PCTs.
References [1] Nakane M, Tamura A, Nagaoka T, Hirakawa K. MR detection of secondary changes remote from ischemia: preliminary observations after occlusion of the middle cerebral artery in rats. Am J Neuroradiol 1997;18:945–50. [2] Koshinaga M, Whittemore SR. The temporal and spatial activation of microglia in fiber tracts undergoing anterograde and retrograde degeneration following spinal cord lesion. J Neurotrauma 1995;12:209– 22. [3] Becerra JL, Puckett WR, Hiester ED, et al. MR-pathologic comparisons of Wallerian degeneration in spinal cord injury. Am J Neuroradiol 1995;16:125–33. [4] Savoiardo M, Pareyson D, Grisoli M, et al. The effects of Wallerian degeneration of the optic radiations demonstrated by MRI. Neuroradiology 1992;34:323–5. [5] Sawlani V, Gupta RK, Singh MK, Kohli A. MRI demonstration of Wallerian degeneration in various intracranial lesions and its clinical implications. J Neurol Sci 1997;146:103–8. [6] Hanihara T, Amano N, Takahashi T, Itoh Y, Yagishita S. Hypertrophy of the inferior olivary nucleus in patients with progressive supranuclear palsy. Eur Neurol 1998;39:97–102. [7] Shepherd GM, Tauboll E, Bakke SJ, Nyberg Hansen R. Midbrain tremor and hypertrophic olivary degeneration after pontine hemorrhage. Mov Disord 1997;12:432–7. [8] Yamamoto T, Yamashita M. Thalamo-olivary degeneration in a patient with laryngopharyngeal dystonia. J Neurol Neurosurg Psychiatry 1995;59:438–41. [9] Sakai T, Matsuda H, Watanabe N, Kamei A, Takashima S. Olivocerebellar retrograde trans-synaptic degeneration from the lateral cerebellar hemisphere to the medial inferior olivary nucleus in an infant. Brain Dev 1994;16:229–32. [10] Uchino A, Hasuo K, Uchida K, et al. Olivary degeneration after cerebellar or brain stem haemorrhage: MRI. Neuroradiology 1993;35:335–8. [11] Revel MP, Mann M, Brugieres P, Poirier J, Gaston A. MR appearance of hypertrophic olivary degeneration after contralateral cerebellar hemorrhage [see comments]. Am J Neuroradiol 1991;12:71–2. [12] Abrahams PH, Day A, Allt G. The node of Ranvier in early Wallerian degeneration: a freeze-fracture study. Acta Neuropathol Berl 1981;54:95–100. [13] Bruck W, Friede RL. The role of complement in myelin phagocytosis during PNS Wallerian degeneration. J Neurol Sci 1991;103:182–7. [14] Berry I, Ranjeva JP, Manelfe C, Clanet M. MRI visualization of multiple sclerosis lesions. Rev Neurol Paris 1998;154:607–17. [15] Ono J, Harada K, Mano T, Sakurai K, Okada S. Differentiation of dys- and demyelination using diffusional anisotropy. Pediatr Neurol 1997;16:63–6. [16] Richards TL, Alvord Jr EC, He Y, et al. Experimental allergic encephalomyelitis in non-human primates: diffusion imaging of acute and chronic brain lesions. Mult Scler 1995;1:109–17.
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203 [17] Ono J, Harada K, Takahashi M, et al. Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res 1995;671:141–8. [18] Maeshima S, Ueno M, Boh-Oka S, Ueyoshi A. Medial medullary infarction: a role of diffusion-weighted magnetic resonance imaging for stroke rehabilitation. Am J Phys Med Rehabil 2002;81: 626–8. [19] Kumral E, Afsar N, Kirbas D, Balkir K, Ozdemirkiran T. Spectrum of medial medullary infarction: clinical and magnetic resonance imaging findings. J Neurol 2002;249:85–93. [20] Kumral E, Bayulkem G, Akyol A, et al. Mesencephalic and associated posterior circulation infarcts. Stroke 2002;33:2224–31. [21] Kim JS. Recurrent pontine base infarction: a controlled study. Cerebrovasc Dis 2002;13:257–61. [22] Fitzek S, Fitzek C, Urban PP, et al. Time course of lesion development in patients with acute brain stem infarction and correlation with NIHSS score. Eur J Radiol 2001;39:180–5. [23] Miyai I, Suzuki T, Kii K, Kang J, Kubota K. Wallerian degeneration of the pyramidal tract does not affect stroke rehabilitation outcome. Neurology 1998;51:1613–6. [24] Brodal P, Bjaalie JG. Organization of the pontine nuclei. Neurosci Res 1992;13:83–118.
203
[25] Nieuwenhuys R, Voogd J, van Huijzen C. The human central nervous system. 3rd ed. Berlin: Springer, 1988. [26] Teixeira RA, Li LM, Santos SL, et al. Crossed cerebellar atrophy in patients with precocious destructive brain insults. Arch Neurol 2002;59:843–7. [27] Bouchareb M, Moulin T, Cattin F, et al. Wallerian degeneration of the descending tracts. CT and MRI features of the brain stem. J Neuroradiol 1988;15:238–52. [28] Stovring J, Fernando LT. Wallerian degeneration of the corticospinal tract region of the brain stem: demonstration by computed tomography. Radiology 1983;149:717–20. [29] Kang DW, Chu K, Yoon BW, et al. Diffusion-weighted imaging in Wallerian degeneration. J Neurol Sci 2000;178:167–9. [30] Kazui S, Kuriyama Y, Sawada T, Imakita S. Very early demonstration of secondary pyramidal tract degeneration by computed tomography. Stroke 1994;25:2287–9. [31] Becerra JL, Puckett WR, Hiester ED, et al. MR-pathologic comparisons of Wallerian degeneration in spinal cord injury. Am J Neuroradiol 1995;16:125–33. [32] Pierpaoli C, Barnett A, Pajevic S, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001;13:1174–85.
Bilateral Wallerian degeneration of the medial cerebellar peduncles after ponto-mesencephalic infarction Clemens Fitzek a,b,∗ , Sabine Fitzek c,d , Peter Stoeter a b
a Institute of Neuroradiology, University of Mainz, Mainz, Germany Department of Diagnostic and Interventional Radiology, Friedrich Schiller University of Jena, Jena, Germany c Department of Neurology, University of Mainz, Mainz, Germany d Department of Neurology, Friedrich Schiller University of Jena, Jena, Germany
Received 18 February 2003; received in revised form 7 April 2003; accepted 9 April 2003
Abstract Three patients with acute large paramedian ponto-mesencephalic infarctions developed a bilateral retrograde degeneration of the medial cerebellar peduncles within 4 months after the insult. In an initial magnetic resonance imaging (MRI) within the first 2 weeks, the medial cerebellar peduncles showed normal intensities, but a control MRI after 4 months showed bright hyperintensities in the T2-TSE weighted images, and moderately increased signal intensities in echo planar imaging–diffusion weighted imaging were seen, possibly representing bilateral Wallerian degeneration of the cerebellar-pontine fibers. © 2003 Elsevier Ireland Ltd. All rights reserved. Keywords: Brain stem; MRI; Diffusion weighted imaging; Wallerian degeneration
1. Introduction
2. Patients and methods
Wallerian degeneration of the tractus pyramidalis after lesions of the motor cortex or the brainstem is well described [1–4] and independently of the kind of lesion, specific magnetic resonance imaging (MRI) signal changes develop in the corticospinal tract during the following months [5]. After peripheral and central lesions Wallerian degeneration is described such as degeneration within the optic nerves after lateral geniculate body lesion [4] or olivary degeneration after intracranial haemorrhage or trauma [6–11]. In Wallerian degeneration myelinated fibres show a loss of the cytoplasmic circumferential bands and longitudinal columns and their associated membrane pores [12]. Macrophage recruitment for myelin removal also takes place [13]. These changes of demyelination lead to signal increase in T2-weighted images (T2w), which is also measurable by diffusion weighted imaging (DWI) [14–17].
2.1. Patients
∗ Corresponding author. Tel.: +49-3641-93-5376; fax: +49-3641-93-6767. E-mail address: [email protected] (C. Fitzek).
Three patients with acute paramedian ponto-mesencephalic brainstem infarction and consequent degeneration of the medial cerebellar peduncle were included. 2.2. CT/MRI Computer tomography (CT) scan without application of contrast medium was performed immediately after admission of the patient to hospital. Up to three MRI were performed: the first MRI (MR0) in the first day after onset of symptoms or admission of the patient to hospital (echo planar imaging (EPI) DWI: TR/TE = 4000/103 ms, with separately applied diffusion-gradients in three spatial axis, b = 1164 s/mm3 , 128 matrix, 250 ms per slice, 20 slices, thickness 3 mm, 8 measurements). The slice orientation was perpendicular to the sagittal brainstem cuts. The second MRI (MR1) was performed within the first 2 weeks after the infarction (T2w-TSE: TR/TE = 3810/90 ms, 256 matrix, thickness 3 mm, T1w: TR/TE = 600/14 ms, 256 matrix, thickness 3
0720-048X/$ – see front matter © 2003 Elsevier Ireland Ltd. All rights reserved. doi:10.1016/S0720-048X(03)00132-3
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
199
Fig. 1. Fifty-nine years old female patient (patient 1) with acute ponto-mesencephalic infarction and increased signal in DWI (a) one day after onset of symptoms. At the same time no lesion of the middle cerebellar peduncle visible in T2w-TSE (b). In the control MRI after 4 months bright signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d). Delineation of the left sided paramedian infarction in control MRI in T2w-TSE (e), with a second contralateral paramedian area of increased signal not present on first examination, which possibly represents Wallerian degeneration.
200
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
mm). The control MRI (MR2) was performed 4 months later with T2w-TSE (TR/TE = 3810/90 ms, 256 matrix, thickness 3 mm). The DWI signal was regarded as hyperintense only when it was increased in all three im-
ages with direction-selective gradient application. The apparent diffusion coefficient (ADC) values were postprocessed off line and were calculated based on the Stejskal–Tanner-equation.
Fig. 2. Sixty-two years old female patient (patient 2) with acute ponto-mesencephalic infarction with increased signal in DWI (a) but normal middle cerebellar peduncles at that time (b). In control MRI after 4 months increased signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d) and sharply deliniated infarction in T2w-TSE (e).
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
201
Fig. 3. Seventy-three years old male patient (patient 3) with a well delineated mesencephalic infarction in the T2w-TSE sequence (a), but normal middle cerebellar peduncles (b). The control MRI after 4 months of symptom onset shows increased signal of the middle cerebellar peduncle of both sides in DWI (c) and T2w-TSE (d).
3. Results 3.1. General characteristics There were three patients one men and two women (age 73, 62, 59 years) with acute ponto-mesencephalic paramedian brain stem infarctions. All three patients had initial symptoms of gait ataxia, dysarthria and contralateral hemiparesis with good improvement during the following 4–5 months. At the follow up only mild gait disturbance and slight hemiparesis was found.
toms indicated the acute stage of the brain stem infarction in the initially scans. In all cases, the medial cerebellar peduncles were normal. In the follow up MRI after 4 months after stroke onset, all three patients developed bright hyperintensities along both medial cerebellar peduncles in the EPI–DWI and the T2w sequences (Figs. 1–3). In two patients the ADC values were slightly decreased compared to the normal, unaffected cerebellar tracts of the inferior and superior peduncles (7.99 × 10−4 mm2 /s vs. 8.05 × 10−4 mm2 /s and 6.87 × 10−4 mm2 /s vs. 8.59 × 10−4 mm2 /s) and in one patient increased ADC values (10.67 × 10−4 mm2 /s vs. 7.39 × 10−4 mm2 /s) were measured.
3.2. MRI In the acute phase all three patients had large paramedian ponto-mesencephalic stroke lesions covering the crossing area of the medial cerebellar peduncle fibers. All three lesions showed bright signal in EPI–DWI. The signal increase in EPI–DWI together with the acute onset of symptoms and the accordance of the lesions to the clinical symp-
4. Discussion We describe three patients with first time acute brain stem stroke and corresponding large unilateral paramedian ponto-mesencephalic ischemic brain stem lesions. The majority of brain stem infarctions do not cross the midline
202
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203
[18–20]. Only in few cases, especially in basilar artery thrombosis, bilateral brain stem infarctions may occur [19–21]. Brain stem infarctions, except those due to basilary thrombosis, have a good prognosis concerning the clinical outcome [22]. Wallerian degeneration does not seem to be a marker for a bad outcome in general [23], and the three patients of our study improved clinically. The middle cerebellar peduncles (brachium pontis) contain the ponto-cerebellar tract (PCT) fibers. These fibers arise from the contralateral pontine nuclei (secondary neurons) which receive collaterals from cortico-pontine tracts. The ponto-cerebellar fibers cross at an upper pontine level [24,25]. Crossed cerebellar atrophy after supratentorial lesions concerning the cortico-pontine tract is well described [26,27]. In the three patients of this series a large unilateral paramedian lesion covered the crossing area of the ponto-cerebellar fibers which become the medial cerebellar peduncle. Consequently both the fiber tracts were affected, one proximally and the other one distally to the decussatio (Fig. 4). In Wallerian degeneration the affected tracts are seen hypointense in CT [28] and show increased signal in T2w MR images and also in DWI [14–17,29] as in our three cases. Wallerian degeneration can be seen histologically a few days after the lesion [30,31]. There are case reports that DWI can show signal increase in affected areas as soon as 12 days after stroke [29]. Our patients showed remaining signal increase in DWI and T2w after 4 months after stroke onset. Water diffusion changes in Wallerian degeneration can be measured with diffusion tensor imaging, too. There seems to be a dependence on white matter architecture were diffusion anisotropy is especially reduced in regions were white matter fibers are arranged in parallel bundles [32]. Our patients showed the described high signal in DWI mainly in the pontine and proximal cerebellar portions of the middle cerebellar tract, were the fibers run predominantly parallel. The reason for the signal increase of T2w or hypodensity in CT probably is due to increased accumulation of water [28,30,31], whereas the reason for the signal increase of the
Fig. 4. Schematic drawing of the tracts (dashed lines): Cortico-pontine and cortico-spinal tracts (TP) including those from the motor cortex (MC) give collaterals to the pontine nuclei (PN). The ponto-cerebellar fibers originate from these nuclei, cross at an upper pontine level and reach the cerebellum through the middle cerebellar peduncles (MCP). A large paramedian lesion (gray area) will affect both MCPs.
DWI with partially decreased, partially elevated ADC-values remains speculative: cell swelling, demyelinisation with axonal degeneration, phagocytotic activity and water uptake are possibly involved [13–17].
5. Conclusion Large paramedian lesions which cover the crossing zone of the medial cerebellar peduncles can lead to a bilateral Wallerian degeneration of the PCTs.
References [1] Nakane M, Tamura A, Nagaoka T, Hirakawa K. MR detection of secondary changes remote from ischemia: preliminary observations after occlusion of the middle cerebral artery in rats. Am J Neuroradiol 1997;18:945–50. [2] Koshinaga M, Whittemore SR. The temporal and spatial activation of microglia in fiber tracts undergoing anterograde and retrograde degeneration following spinal cord lesion. J Neurotrauma 1995;12:209– 22. [3] Becerra JL, Puckett WR, Hiester ED, et al. MR-pathologic comparisons of Wallerian degeneration in spinal cord injury. Am J Neuroradiol 1995;16:125–33. [4] Savoiardo M, Pareyson D, Grisoli M, et al. The effects of Wallerian degeneration of the optic radiations demonstrated by MRI. Neuroradiology 1992;34:323–5. [5] Sawlani V, Gupta RK, Singh MK, Kohli A. MRI demonstration of Wallerian degeneration in various intracranial lesions and its clinical implications. J Neurol Sci 1997;146:103–8. [6] Hanihara T, Amano N, Takahashi T, Itoh Y, Yagishita S. Hypertrophy of the inferior olivary nucleus in patients with progressive supranuclear palsy. Eur Neurol 1998;39:97–102. [7] Shepherd GM, Tauboll E, Bakke SJ, Nyberg Hansen R. Midbrain tremor and hypertrophic olivary degeneration after pontine hemorrhage. Mov Disord 1997;12:432–7. [8] Yamamoto T, Yamashita M. Thalamo-olivary degeneration in a patient with laryngopharyngeal dystonia. J Neurol Neurosurg Psychiatry 1995;59:438–41. [9] Sakai T, Matsuda H, Watanabe N, Kamei A, Takashima S. Olivocerebellar retrograde trans-synaptic degeneration from the lateral cerebellar hemisphere to the medial inferior olivary nucleus in an infant. Brain Dev 1994;16:229–32. [10] Uchino A, Hasuo K, Uchida K, et al. Olivary degeneration after cerebellar or brain stem haemorrhage: MRI. Neuroradiology 1993;35:335–8. [11] Revel MP, Mann M, Brugieres P, Poirier J, Gaston A. MR appearance of hypertrophic olivary degeneration after contralateral cerebellar hemorrhage [see comments]. Am J Neuroradiol 1991;12:71–2. [12] Abrahams PH, Day A, Allt G. The node of Ranvier in early Wallerian degeneration: a freeze-fracture study. Acta Neuropathol Berl 1981;54:95–100. [13] Bruck W, Friede RL. The role of complement in myelin phagocytosis during PNS Wallerian degeneration. J Neurol Sci 1991;103:182–7. [14] Berry I, Ranjeva JP, Manelfe C, Clanet M. MRI visualization of multiple sclerosis lesions. Rev Neurol Paris 1998;154:607–17. [15] Ono J, Harada K, Mano T, Sakurai K, Okada S. Differentiation of dys- and demyelination using diffusional anisotropy. Pediatr Neurol 1997;16:63–6. [16] Richards TL, Alvord Jr EC, He Y, et al. Experimental allergic encephalomyelitis in non-human primates: diffusion imaging of acute and chronic brain lesions. Mult Scler 1995;1:109–17.
C. Fitzek et al. / European Journal of Radiology 49 (2004) 198–203 [17] Ono J, Harada K, Takahashi M, et al. Differentiation between dysmyelination and demyelination using magnetic resonance diffusional anisotropy. Brain Res 1995;671:141–8. [18] Maeshima S, Ueno M, Boh-Oka S, Ueyoshi A. Medial medullary infarction: a role of diffusion-weighted magnetic resonance imaging for stroke rehabilitation. Am J Phys Med Rehabil 2002;81: 626–8. [19] Kumral E, Afsar N, Kirbas D, Balkir K, Ozdemirkiran T. Spectrum of medial medullary infarction: clinical and magnetic resonance imaging findings. J Neurol 2002;249:85–93. [20] Kumral E, Bayulkem G, Akyol A, et al. Mesencephalic and associated posterior circulation infarcts. Stroke 2002;33:2224–31. [21] Kim JS. Recurrent pontine base infarction: a controlled study. Cerebrovasc Dis 2002;13:257–61. [22] Fitzek S, Fitzek C, Urban PP, et al. Time course of lesion development in patients with acute brain stem infarction and correlation with NIHSS score. Eur J Radiol 2001;39:180–5. [23] Miyai I, Suzuki T, Kii K, Kang J, Kubota K. Wallerian degeneration of the pyramidal tract does not affect stroke rehabilitation outcome. Neurology 1998;51:1613–6. [24] Brodal P, Bjaalie JG. Organization of the pontine nuclei. Neurosci Res 1992;13:83–118.
203
[25] Nieuwenhuys R, Voogd J, van Huijzen C. The human central nervous system. 3rd ed. Berlin: Springer, 1988. [26] Teixeira RA, Li LM, Santos SL, et al. Crossed cerebellar atrophy in patients with precocious destructive brain insults. Arch Neurol 2002;59:843–7. [27] Bouchareb M, Moulin T, Cattin F, et al. Wallerian degeneration of the descending tracts. CT and MRI features of the brain stem. J Neuroradiol 1988;15:238–52. [28] Stovring J, Fernando LT. Wallerian degeneration of the corticospinal tract region of the brain stem: demonstration by computed tomography. Radiology 1983;149:717–20. [29] Kang DW, Chu K, Yoon BW, et al. Diffusion-weighted imaging in Wallerian degeneration. J Neurol Sci 2000;178:167–9. [30] Kazui S, Kuriyama Y, Sawada T, Imakita S. Very early demonstration of secondary pyramidal tract degeneration by computed tomography. Stroke 1994;25:2287–9. [31] Becerra JL, Puckett WR, Hiester ED, et al. MR-pathologic comparisons of Wallerian degeneration in spinal cord injury. Am J Neuroradiol 1995;16:125–33. [32] Pierpaoli C, Barnett A, Pajevic S, et al. Water diffusion changes in Wallerian degeneration and their dependence on white matter architecture. Neuroimage 2001;13:1174–85.