The Neuroradiology Journal 19: 589-596, 2006

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MRI Findings in Patients with Hemiparetic Cerebral Palsy M. KOROGLU*, A. TUREDI**, N. KISIOGLU***, I. ILHAN ERGURHAN** * Department of Radiology, ** Department of Pediatrics, *** Department of Public Health, Suleyman Demirel University, School of Medicine; Isparta, Turkey

Key words: hemiparetic cerebral palsy, etiology, computed tomography, magnetic resonance imaging, children, CNS malformation

SUMMARY – Given the more severe and extensive unilateral brain abnormalities in hemiparetic cerebral palsy (HCP) patients than in other spastic cerebral palsy patients we focused exclusively on the localization of brain lesions in children with HCP. The relationship between neuroradiological findings and side of hemiparesis was investigated in a group of 30 children with HCP. Seventeen boys and 13 girls aged four to18 years (mean age 9.7±4.2 years) were included in this study. Computed tomography and magnetic resonance imaging examinations were correlated with the birth histories, obstetrical records and clinical summaries. Of the 30 patients with HCP, 2 (6.6%) had normal neuroradiological examinations, 20 (66.6%) had unilateral and eight (26.6%) bilateral brain lesions. A brain lesion on the contralateral side of hemiparesis was found in 93.3% of the neuroradiological examinations. The commonest neuroradiological findings in our study were periventricular leukomalacia (PVL, 80%), atrophy (70%) and porencephalic cyst (50%). There was a significant relationship between the symptomatic side and contralateral PVL, atrophy and porencephalic cyst (40%). PVL, atrophy and porencephalic cyst were significantly concomitant on the same side (46.6%). We demonstrated for the first time in the literature that PVL, atrophy and porencephaly are usually observed concomitantly and contralateral to the side of motor impairement in HCP patients.

Introduction Cerebral palsy (CP) describes a group of motor impairment syndromes secondary to genetic or acquired disorders of the developing brain 1. Hemiparetic cerebral palsy (HCP) is defined as CP with a unilateral motor disorder 2. CP and its mechanisms are still not fully understood. In children with hemiparetic cerebral palsy neuroradiological imaging has become an important determinant of diagnosis and management. Although there is often a relationship between the type and severity of neuroradiological imaging abnormalities and degree of clinical impairment, exceptions exist 3. Unfortunately, little information is available on the relationship between neuroradiological abnormalities and side of hemiparesis in HCP patients. The

relationship between neuroradiological imaging abnormalities and the infants’ clinical outcome, especially the side of hemiparesis remain to be more thoroughly elucidated. The objective of this study was to localize the brain lesion in HCP with the neuroradiological imaging modalities. Methods The study was approved by the local Ethical Committee. We reviewed computed tomography (CT) and magnetic resonance imaging (MRI) findings of a consecutive group of 30 patients diagnosed with HCP. Inclusion criteria were the presence of HCP and the availability of a brain MR imaging study. Children with 589

MRI Findings in Patients with Hemiparetic Cerebral Palsy

mixed (pyramidal and extrapyramidal) CP and diplegic CP were excluded. All of the patients were referred to our center, a university hospital, by different pediatricians especially for parent counseling. Neuroradiological examinations were compared with the birth histories, obstetric records and clinical summaries. Maternal history of previous abortions and neonatal mortality, family history of consanguinity, CP, retarded development or CNS malformation in close relatives were questioned. During pregnancy physical malformation unrelated to the CNS, low birth weight (LBW), multiple gestation, abnormal fetus, chronic maternal disease, imminent abortion, hemorrhages during pregnancy and abortive attempts were also questioned. Any perinatal insult such as, prematurity, chorioamnionitis, early detachment of the placenta, intracranial hemorrhage, metabolic disturbances, hypotension, persistent respiratory distress, mechanical ventilation and infection were also recorded. In this study, the term “birth asphyxia” is used for failure to initiate and sustain breathing at birth, since there is no agreement on a more precise definition. Epilepsy is defined as propensity for an individual to have recurrent, unprovoked epileptic seizures. The diagnosis of epilepsy was made when a patient had at least two unevoked seizures. Seizures during the neonatal period were excluded. Axial images parallel to the canthomeatal line were obtained using a 5mm slice thickness in CT imaging. CT images were reviewed with a window width of 125 and window level of 65. In MR imaging a sagittal T1-weighted sequence was performed in all patients. This sequence allowed assessment of the midline structures that are frequently abnormal in congenital brain malformations. Repetition time (TR) for this sequence was 600 ms, echo time (TE) was 20ms, slice thickness was 5 mm with 1 mm gap; 192×256 matrix was used with one excitation. After sagittal images acquisition, axial T1weighted and axial, coronal T2-weighted images were obtained. Imaging parameters identical to those for sagittal T1-weighted images were used for T1-weighted axial images. For T2-weighted sequences, spin echo sequences with a 5 mm slice thicknesss, 2 mm gap, TR of 3000 ms, TE of 60 ms (first echo) and 90 ms (second echo), 196×256 acquisition matrix and one excitation was used. 590

M. Koroglu

Fluid attenuated inversion recovery (FLAIR) sequence was obtained with a TR of 10000 ms, TE of 100 ms, inversion time of (TI) 2200 ms, with 3 mm contiguous slices and 192 phase encoding steps. The images were assessed for abnormal volume and signal within the white and cortical gray matter, the basal ganglia, thalami and cerebellum. The degree of myelination and ventricular size were routinely assessed. Any other abnormalities such as cysts or migrational abnormalities were also documented. Statistical analysis was performed using the SPSS statistical package (Version 9.0, SPSS Inc., Chicago, IL, USA) for Windows. Chisquare test was used to determine the differences between the side of hemiplegia and neuroradiological lesions, non parametric two independent sample test (Mann-Whitney U) was used to determine the relation between age and lesion types. All reported P-values are two tailed. A P-value of 0.05 was considered statistically significant. Results Thirty HCP patients (17 boys and 13 girls) aged four to18 years (mean age 9.7 ± 4.2 years) were included in this study. Mean age of the patients at the time of neuroradiological examinations was 3.88 ± 3.69 years (range 3 months to 14 years). Gestational age of our patients varied between 31 to 41 weeks (mean 38.9 ± 2.7 weeks). Birth weight of our patients varied between 1400 and 4750 grams (mean 2950 ± 815.1grams). A wide variety of prenatal and perinatal histories were present. Of the 30 patients with HCP, two (6.6%) had normal neuroradiological examinations, 20 (66.6%) had unilateral and eight (26.6%) bilateral brain lesions. A brain lesion was found in 28 (93.3%) of the 30 CT and MRI examinations on the contralateral side of hemiparesis. The commonest neuroradiological findings in our study were PVL (24/30, 80%), atrophy (21/30, %70) and porencephalic cyst (15/30, 50%), (figure 1-3). Infarcts (5/30, 16.6%), subdural effusions (3/30, 10%) and congenital CNS anomalies (4/30, 13.3%) were the other pathologies. There was no significant difference between right and left HCP patients with respect to lesions (PVL, atrophy, porencephalic cyst, infarct, subdural effusion and congenital CNS anomalies) and lesion frequencies. Table 1

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A

The Neuroradiology Journal 19: 589-596, 2006

B

Figure 1 Left periventricular leukomalacia in a 6-year-old boy with right hemiparetic cerebral palsy. T2-weighted axial (A) and coronal (B) images demonstrate hyperintensity in the periventricular white matter (arrows).

A

B

Figure 2 Right periventricular leukomalacia in a 2-year-old boy with left hemiparetic cerebral palsy. T2-weighted axial (A) image demonstrate irregularity and dilataton of the lateral ventricule (arrow), and atrophy of right cerebral cortex. T1-weighted sagittal (B) image demonstrate thinning of the corpus callosum (arrow).

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MRI Findings in Patients with Hemiparetic Cerebral Palsy

M. Koroglu

A

B

Figure 3 Right porencephalic cyst in an 11-year-old boy with left hemiparetic cerebral palsy. T1-weighted axial images demonstrate smooth-walled cavity (arrows) communicating with a lateral ventricle with loss of surrounding brain parenchyma in the right temporoparietal region.

Table 1 Side of hemiparetic cerebral palsy and brain lesion

Ipsilateral brain lesion

Contralateral brain lesion

Bilateral brain lesion



8 (72.7%)

3 (27.3%)

1 (7.7%)

8 (61.5%)

4 (30.8%)

8 left HCP patients



7 (87.5%)

1 (12.5%)

13 right HCP patients



12 (92.3%)

1 (9.1 %)

1 (20%)

4 (80%)





10 (100%)



Periventricular leukomalacia 11 left HCP patients 13 right HCP patients Atrophy

Porencephalic cyst 5 left HCP patients 10 right HCP patients

summarizes the significant relationship between the side of HCP and PVL, atrophy and porencephalic cyst (p = 0.001, p < 0.000, p = 0.001 respectively). A set of concomitant neuroradiological find592

ings (PVL, atrophy and porencephalic cyst) was seen in 46.6% (14/30) of patients. This combination was usually (12/30, 40%) contralateral to motor impairment (p=0.013). In one patient with right HCP, PVL was located on the right

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The Neuroradiology Journal 19: 589-596, 2006

A

B

Figure 4 Left porencephalic cyst, bilateral atrophy and periventricular leukomalacia in a 1-year-old girl with left hemiparetic cerebral palsy. FLAIR axial images demonstrate smooth-walled left porencephalic cyst (arrow) communicating with a lateral ventricle and bilateral hyperintensity in the periventricular white matter (open arrows). The volume of white matter is also markedly decreased especially on the right side.

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Table 2 Neuororadiological imaging findings in epileptic and non-epileptic hemiparetic cerebral palsy patients

Epileptic CP (n: 7)

Non-epileptic CP (n:23)

P*

Normal

0

2

0.494

PVL

6

18

0.666

Atrophy

5

16

0.925

Porencephalic cyst

3

12

0.666

Infarct

1

4

0.846

Subdural effusion

0

3

0.773

Congenital anomalies

3

1

0.030**

CP: cerebral palsy PVL: Periventricular leukomalacia *: chi square test - **: Fisher’s exact test

side of the brain, atrophy and porencephalic cyst were located on the left side. In another patient with left HCP, porencephalic cyst was located on the left side and atrophy and PVL were bilateral (figure 4). A combination of these neuroradiological findings was seen at a significantly higher rate in premature patients (p = 0.027). Frequencies of neuroradiological lesions were analysed according to the patient’s age during the neuroradiological examination. Mean age of subdural effusion patients (3/30) was 7.3 months (range 3-12 months) during neuroradiological examination. Subdural effusion was observed to a greater extent in patients with an early neuroradiological examination (MannWhitney U test, p = 0.012). The incidence of epilepsy in our study was 23.3%. We also studied the occurrence of epilepsy in HCP patients and the relationship of epilepsy with specific types of brain lesions (table 2). The percentage of patients with epilepsy was significantly high among those with congenital anomaly (p = 0.009). Discussion We noticed that the unilateral abnormal findings in the brain were more severe and more extensive in HCP patients than in other spastic CP patients, and therefore we focused exclusively on the localization of brain lesions in children with HCP. Great progress has been made in relation to imaging in HCP, only 8% to 24% of the examinations being reported as normal 2,4. A high rate 594

of positive findings has been reported in the literature 5-9. For parents seeking a cause for their child’s disability, a radiological diagnosis is now possible in the majority of cases. Recent studies, based on neuroimaging findings, provide objective information, elucidating and classifying the etiology of CP more clearly 2,10 . The pattern of brain injury of patients with CP is closely related to the gestational age of occurrence. Typical preterm brain injuries include PVL and post-hemorrhagic porencephaly. Periventricular leukomalacia usually occurs between 28 and 34 weeks of gestation and is caused by an ischemic process in the watershed zone that exists in the periventricular white matter of the immature brain 5,6. Selective vulnerability of the immature cerebral blood vessels and oligodendroglia in the periventricular white matter to fluctuations in cerebral perfusion and to oxygen free radicals is thought to be responsible for this specific pattern of brain injury in the preterm neonate 2,11-13. Findings of PVL are related to injury to developing periventricular white matter during the late second and early third trimesters of pregnancy 11,14-17. After about 34 weeks of gestation, subcortical and cortical areas are the most vulnerable regions of the brain for hypoxic-ischemic insult and the resulting lesions include subcortical leukomalacia, multicystic encephalamalacia and gliosis 5-7,18. Over the last few decades, prenatal etiology has been confirmed based on neuropathological studies and more recently using MRI 2,4,19,20. Steinlin et al analysed the MRI findings of 33 children with congenital hemiplegia and their data suggested a prenatal origin in 20 to 40%

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of cases 6. These data could partly explain why the incidence of congenital hemiplegia has not decreased during the last decades, despite advances in perinatal and neonatal care 21,22. The neuroradiological imaging findings were predictive of subtypes of CP 16. Hemorrhagic venous infarction or grade IV hemorrhage in severe cases of subependymal hemorrhage and extensive cerebral infarction on early MRI examinations both led to HCP 16. Periventricular leukomalacia was the most predominant MRI finding after the first year of life in HCP patients as demonstrated in our study 19. Okumura et Al studied MRI in children who had CP and related the findings to the gestational age at birth and the type of CP. They found that the relationship was significant and that about two thirds of the patients with HCP had unilateral lesions and infarct of the middle cerebral artery territory, as well as hemiatrophy resulting from leukomalacia 18. In cases of HCP which occur in full term infants, the most common finding is a lesion in the area of the middle cerebral artery mainly the left one and this factor is not described for the other types of CP 18,23. In our series a combination of neuroradiological findings, namely PVL, atrophy and porencephalic cyst, was seen at a significantly higher rate in premature patients. The contribution of congenital infection to the total number of children with CP remains uncertain. In a series of 489 cases with spastic CP, congenital infection was considered to be the major etiological factor in only 3.3% 5,7. Congenital toxoplasma infection was detected in one of our patients. Wiklund et Al showed that 17% of the HCP cases had central nervous system malformations (CNS-MF) 3. Four patients in our series had CNS-MF. The neuronal migration anomalies demonstrated in our study were schizencephaly and heterotopia indicating insults during the second trimester of pregnancy. Other malformations were tuberous sclerosis (TS) and Dyke-Davidoff-Masson syndrome. The clinical features of Dyke-Davidoff-Masson syndrome (cerebral hemiatrophy) include facial asymme-

The Neuroradiology Journal 19: 589-596, 2006

try, seizures and HCP 24. Patients with CP may have some problems other than motor impairment. Epilepsy often worsens the quality of life of patients with CP 25. It has been estimated that approximately 20% of cases of childhood epilepsy are the result of brain lesions that are also the cause of CP 25. There have been some reports indicating that the risk of epilepsy varies in different subtypes of CP. The occurrence of epilepsy is high in patients with quadriplegia and low in those with diplegia 26. These facts suggest that the occurrence of epilepsy is likely to be related to the type of brain lesions. It is still unknown why apparently identical lesions may or may not cause seizures 25. However, the relationship between epilepsy and the type of brain lesions is not fully understood. The percentage of patients with epilepsy was significantly high among those with congenital anomaly in our series. Finally, a potential limitation of this study is its retrospective nature. Another diagnostic limitation is that chronic brain injuries were imaged with these late neuroradiologic imaging studies. Conclusion We have described our findings in a consecutive series of neuroradiological examinations performed to localize the brain lesion of HCP patients. Localization of the brain lesion may improve parent counseling and promote timely implementation of intervention programs. The morphological information obtained by neuroradiological examinations was found to be useful for predicting clinical outcome, and was considered an important adjunct to clinical history and findings in these children. PVL, atrophy and porencephaly are all manifestations of cerebral tissue loss and a relationship is expected. We have demonstrated that PVL, atrophy and porencephaly are usually observed in combination and contralateral to the side of motor impairment in HCP patients.

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18 Okumura A, Hayakawa F, Kato T et Al: MRI findings in patients with spastic cerebral palsy. I. correlation with gestational age at birth. Dev Med Child Neurol 39: 363-368, 1997. 19 Niemann G, Wakat JP, Krageloh-Mann I et Al: Congenital hemiparesis and periventricular leukomalacia: pathogenetic aspects on magnetic resonance imaging. Dev Med Child Neurol 36: 943-950, 1994. 20 Bouza H, Dubowitz LMZ, Rutherford M et Al: Late magnetic resonance imaging and clinical finding in neonates with unilateral lesions on cranial ultrasound. Dev Med Child Neurol 36: 951-954, 1994. 21 Kwong KL, Wong YC, Fong CM et Al: Magnetic resonance imaging in 122 children with spastic cerebral palsy. Pediatr Neurol 31: 172-176, 2004. 22 Bottos M, Granato T, Allibrio G et Al: Prevalence of cerebral palsy in north east Italy from 1965 to 1989. Dev Med Child Neurol 41: 26-38, 1999. 23 Molteni B, Oleari G, Fedrizzi E et Al: Relation between CT patterns, clinical findings and etiological factors in children born at term, affected congenital hemiparesis. Neropediatrics 18: 75-80, 1987. 24 Tasdemir HA, Incesu L, Yazicioglu AK et Al: DykeDavidoff-Masson syndrome. Clin Imaging 26: 13-17, 2002. 25 Senbil N, Sonel B, Aydin OF et Al: Epileptic and nonepileptic cerebral palsy: EEG and cranial imaging findings. Brain Dev 24: 166-169, 2002. 26 Hadjipanayis A, Hadjichristodoulou C, Youroukos S: Epilepsy in patients with cerebral palsy. Dev Med Child Neurol 39: 659-663, 1997.

Mert Koroglu, M.D. Department of Radiology Süleyman Demirel University School of Medicine 32100 Isparta - Turkey Phone: +90 505 374 44 85 e-mail: [email protected]

MRI findings in patients with hemiparetic cerebral palsy.

Given the more severe and extensive unilateral brain abnormalities in hemiparetic cerebral palsy (HCP) patients than in other spastic cerebral palsy p...
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