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Evaluation of the Intraspinal Enhancement forMedulloblastoma on MR Imaging1

Hwa-Young Kim, M.D., In-One Kim, M.D., Woo Sun Kim, M.D.,Jung-Eun Cheon, M.D., Kyung Mo Yeon, M.D.

Purpose: The purpose of this study was to analyze the enhancement pattern of thespinal cord for patients with medulloblastoma, and to correlate the enhancement pat-tern with cerebrospinal fluid (CSF) tumor seeding.Materials and Methods: We retrospectively reviewed 84 MR images, including the ini-tial and follow-up studies after chemotherapy or radiation therapy, of 25 patients withmedulloblastoma who were aged from 2 to 13 years. We analyzed the spinal lep-tomeningeal enhancement pattern on the MR images. The leptomeningeal enhance-ment patterns were categorized into three types: Type I, fine or discontinuous linearenhancement, and type II, continuous linear or nodular enhancement, and type III, in-tradural mass formation. We correlated the enhancement pattern on MRI with the re-sults of CSF cytology at the initial and follow - up examinations after treatment.Results: Of total 25 patients, type I enhancement was observed for 14 patients. Twelvepatients were negative on the initial CSF cytology and 2 patients were positive. On thefollow-up MR studies, 14 patients showed no change or only a slight decrease of en-hancement, and all were negative on the follow-up CSF cytology. Type II enhance-ment patterns were observed in seven patients, and all of them were positive on theinitial CSF cytology. On follow-up MR study, one patient revealed an increased en-hancement with the positive result on the follow-up CSF cytology, and six patients haddecreased enhancement on the follow-up MR studies with negative conversion on thefollow-up CSF cytology. Type III enhancement patterns were observed in four patientsand all of them were positive on the initial CSF cytology. All four patients with in-tradural mass formations revealed progression of the lesions on follow-up MR studies,and all of them were positive on the follow-up CSF cytology.Conclusion: Type II and III enhancement patterns always represented CSF seedingand a type I enhancement pattern had a low probability of metastasis.

Index words : Brain neoplasmsBrain neoplasms, metabolismBrain, MRSpine, MR

1Department of Radiology and Institute of Radiation Medicine, MRC Seoul National University College of MedicineReceived October 23, 2003 ; Accepted September 14, 2004Address reprint requests to : In-One Kim, M.D., Department of Radiology, Seoul National University Children’s Hospital,28 Yongon-dong, Chongno-gu, Seoul 110-744, Korea.Tel. 82-2-760-3608 Fax. 82-2-747-5781

There are a variety of brain tumors that may seed intothe CSF, and the presence of subarachonoid seeding byneoplasms implies a poor prognosis (1). Medulloblas-toma occurs in the posterior fossa of children and itmost frequently metastasizes through the lep-tomeningeal route. Although CSF cytology has been es-tablished as the definitive traditional means for detect-ing leptomeningeal tumor, a non-invasive imagingmodality that can accurately diagnose the subarachnoidspread of primary intracranial neoplasms would be ben-eficial to clinicians for staging the disease, prescribingtreatment and determining the prognosis. The evalua-tion of the CSF seeding in brain and spine with post-con-trast MR imaging has been studied since the late 1980’s,along with the use of myelography and CT-myelogra-phy, and the pre- and post-enhanced CT scans have alsobeen regarded as useful methods (2, 3). The evaluationof CSF seeding on the initial and follow-up studies forthe early detection of tumor metastasis is important fortherapeutic planning and because of the high rate of re-currence of intracranial lesions.

We retrospectively analyzed the spinal lep-tomeningeal enhancement patterns for patients withmedulloblastoma at initial and follow-up MR studies,and we correlated these findings with the CSF cytologicresults for the intraspinal metastasis.

Materials and Methods

We selected 25 consecutive patients with medulloblas-toma that was confirmed by operation from January in1990 to December in 2000, and the patients included 19boys and 6 girls. The age of patients ranged from 2 to 13years old (mean, 6.8 years old). All patients underwentsuboccipital craniectomy and C1 laminectomy for massexcision, and they received combined chemotherapyand radiotherapy, except for one patient who was lessthan 3 years old.

A total 84 MR imaging studies (an average of 3.4 timesper patient) were performed for the whole spine. Weretrospectively analyzed the spinal MR images thatwere taken during the initial studies and during the fol-low-up studies after the operations for all patients. Theinitial MR examinations were performed about 1-2weeks after the operation in all patients. The follow-upstudies that were done during or after chemo or radia-tion treatment were repeated two to nine times at 4 to48 months (mean: 19 months) with a 4-6 month inter-val. Routine imaging sequences were the sagittal T1

weighted image (TR/TE 600-800/12-14 msec, slicethickness; 3-4 mm contiguous sections through thewhole spine), and the axial T1 weighted image (TR/TE600-800/12-14 msec, slice thickness 7-10 mm). Thesame sequences were used after 0.1 mM / Kg of Gd-DT-PA was injected for contrast enhancement. The MRimaging findings after contrast enhancement were cate-gorized into 3 types by the pattern of leptomeningeal en-hancement. Type I was fine or discontinuous linear en-hancement, type II was continuous linear or nodular en-hancement, and type III was intradural mass formation.The criteria for the thickness of the enhanced lep-tomeninges used for dividing the patterns into type Iand type II imaging findings was the thickness of the pe-ripheral nerve roots on post-contrast axial scan.

CSF cytology examinations for these patients wereperformed within a day after MR examination. We com-pared the MR enhancement pattern with the result of

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Fig. 1. A 2-year-old boy with medulloblastoma.The initial MR image shows fine discontinuous lep-tomeningeal enhancement, a finding which finding was classi-fied as type I, along the surface of the spinal cord in the lowerthoracic spine and upper lumbar spine levels on post-contrastT1 sagittal scan (arrows). The follow-up MR image showsslightly decreased enhancement (not shown). No malignantcells were found at the initial and follow up CSF cytology ex-amination.

CSF cytology. We analyzed the changes of the enhance-ment pattern on MR and the result of CSF cytology atthe follow-up studies.

Results

At the initial MR examinations, the enhancement pat-terns in spinal cord were analyzed as follows; 14 pa-tients had type I, seven patients had type II and four pa-tients had type III. Twelve of 14 patients with type I en-hancement patterns exhibited negative CSF cytologyand two patients revealed positive cytology (Fig. 1). Wecould not find any difference in the MR findings be-tween the negative and positive cytology results. Theenhanced segments with type I enhancement patternswere mainly located from the lower thoracic spine tothe upper lumbar spinal levels. All patients with type II(Fig. 2) and type III (Fig. 3) enhancement patterns werepositive on the initial CSF cytology.

On the follow-up MR studies, seven of 14 patientswith type I enhancement patterns showed no intervalchanges, and the remaining seven patients revealedmild decreases in the extent of enhancement. All pa-tients with type I enhancement patterns were negative

on the follow-up CSF cytology. One of seven patientswith type II enhancement patterns showed progressionof the extent of lesion on the follow-up MR imaging, andthey were still positive on the follow-up CSF cytology.Six of seven patients with type II enhancement patternsshowed decreases in the extent of enhancement of thelesions on the follow-up MR imaging, and they revealednegative conversion of the CSF cytology. Four patientswith type III enhancement patterns revealed progres-sion of lesions on the follow-up MR images. One patientwith type III enhancement patterns showed temporaryregression of lesions at the 4 month follow-up MR imag-ing, but the intradural masses recurred with aggravationon the 13 months follow-up MR imaging. CSF cytologyresults in patients with type III enhancement patternswere positive at the follow-up studies.

Discussion

Metastatic spread of disease in the spinal subarach-noid space may originate from neoplasms arising fromwithin the central nervous system such as cerebralglioblastoma, ependymoma, medulloblastoma and non-CNS tumor (2). Medulloblastoma is the most frequently

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A B CFig. 2. A 5- year-old boy with medulloblastoma.A. The initial post-contrast T1-weighted image shows nodular and linear enhancement (arrows) on the surface of the spinal cord(type II). CSF cytology examination revealed positive results for malignant cells.B. The axial image shows continuous round rim enhancement (arrow) around the spinal cord. The enhanced segment is thickerthan the enhanced peripheral nerve root.C. The follow-up image shows decreased leptomeningeal enhancement (arrows). CSF cytology revealed negative conversion.

metastasized tumor in children, and this spreads via theCSF pathway. Leptomeningeal metastasis in medul-loblastoma can be identified on the initial imaging stud-ies in 10 to 50% of patients, and it is found as recurrentlesion on follow-up images (3). Although CSF cytologyhas been the traditional means of diagnosis for lep-tomeningeal metastasis, non-invasive imaging modali-ties can accurately diagnose the subarachnoid spread ofprimary intracranial neoplasms. Post-contrast MR imag-ing is the superior method for diagnosing subarachnoiddissemination and for monitoring the disease responseto therapy due to its high resolution, the relatively shortevaluation time and fewer artifacts from this modality,the non-invasiveness of the procedure and there are noserious side effects of intravenous Gd-DTPA (4-7). Inchildren who present with acute hydrocephalus andposterior fossa tumor, the danger of herniation oftennegates the possibility of lumbar puncture. Post-contrastMR imaging in this clinical situation is useful because ofits non-invasive nature and ease of performance (8). Inspinal imaging, the sagittal scan is usually used for eval-uation of the subarachnoid space. If evidence of in-tradural extramedullary disease in spine is sought, theT1 weighted sagittal images before and after the en-hancement will be sufficient, and an axial scan can beused as a supplement. T2 weighted images may not be

necessary (8).The leptomeningeal enhancement pattern itself could

be confusing for determine the stage and extent of dis-ease. Both layers of the pia-arachnoid have tight junc-tions within the capillaries and therefore, lep-tomeningeal enhancement is normally not seen or it issubtle following contrast administration for either MRor CT (9, 10). Diffuse or widespread multifocal nodularenhancement and thickened leptomeninges are the typi-cal finding of leptomineningeal metastasis on the post-contrast MR imaging (11, 12). However, this could alsorepresent a non-tumorous condition such as granuloma-tous infection (13). The fine discontinuous linear en-hancement pattern in the leptomeninges of the brain orspine on post-contrast MR has been described as normal(14, 15) or as benign inflammation, such as the patternsthat occurs from bacterial meningitis, sarcoidosis orpostoperative hemorrhage (16, 17). Sze et al (15) andWatanabe (18) have found that Gd-enhanced MR imag-ing was normal in nearly one third of cases with clinical-ly diagnosed meningeal carcinomatosis. They suggestedthat these cases might have been at an early stage, orthey were less severely affected, and that as the diseaseprogresses, diffuse or nodular meninigeal enhancementcould be seen. The median survival time of these pa-tients was, however, longer than the medial survival

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A B

Fig. 3. A 2-year-old boy with medul-loblastoma.A. The initial post-contrast MR imageshows multiple nodular masses in theintradural extramedullary space of thespine (type III). CSF cytology examina-tion was positive.B. The follow-up image after 4 monthsshows markedly decreased enhance-ment, but the results of CSF cytologyexamination was still positive. Finally,the metastasis was aggravated after 9months, and the patient expired.

time of the patients for whom the typical MRI findingsof CSF seeding were seen at the initial examination. Ourpatients with type I enhancement patterns did not expe-rience tumor recurrence during the follow-up period af-ter chemotherapy and radiotherapy, while all the pa-tients with type III enhancement patterns died withinfour years even though they were small in series.

Traditionally, a definitive diagnosis requires the find-ing of malignant cells in CSF cytologic examination, andthis remains the most accurate means for detecting theleptomeningeal tumor. However, several lumbar punc-tures may be required to establish the accurate diagno-sis (19). On occasion, the results of the CSF are equivo-cal despite repeated lumbar punctures because a falsenegative diagnosis may result from strong adherence ofmalignant cells to the leptomeninges. Gd-DTPA en-hanced MR imaging may serve an adjunctive purposehere (8). CSF cytology is more frequently positive in pa-tients with diffuse meningeal involvement (> 75%) thanfor those patients with focal disease (38%), and also forthose patients with the leptomeningeal enhancementpattern than for those patients with the dural enhance-ment pattern (20).

In our study, patients with type II and type III en-hancement patterns presented with subarachnoidmetastasis, but patients with type I enhancement pat-terns showed metastasis, as proven by CSF cytology, inonly 2 of 14 cases (14%), and the remaining 12 cases (86%) were presumed to be benign inflammatory changesdue to chemical reactions of the blood after the opera-tions. Common postoperative findings in the meningesvary from no enhancement to smooth dural enhance-ment, and this may persist for a prolonged period ofyears (9). The possibility of a complicating infection af-ter an operation could be ruled out by the clinical signs.The criteria for differentiating between insignificant (i.e.postoperative) and significant (i.e., neoplastic or inflam-matory) meningeal enhancement have not been estab-lished for the pediatric population (6, 15). The non-tu-morous condition of fine discontinuous enhancement inour cases could be the result of meningeal irritationcaused by postoperative blood in the subarachnoidspace, but the possibility of metastasis could not be ex-cluded. Therapy after operating, including chemothera-py and craniospinal radiation, had been performed inour cases and regular follow-up examinations are rec-ommended.

In conclusion, the type I enhancement patterns with afine discontinuous linear enhancement had a low proba-

bility of seeding, while type II and III enhancement pat-terns always represented CSF seeding. Further studiesare necessary to delineate the difference between the tu-morous condition and the non-tumorous condition ofleptomeningeal enhancement for type I enhancementpatterns.

References

1. Yousem DW, Patrone PM, Grossman RI. Leptomeningeal metas-tases: MR evaluation. J Comput Assist Tomogr 1990;14:255-261

2. Schuknecht B, Huber P, Buller B, Nadjmi M. Spinal lep-tomeningeal neoplastic disease. Evaluation by MR, myelographyand CT myelography. Eur Neurol 1992;32 :11-16

3. Osborn AG. Diagnostic neuroradiology: 2nd ed. St. Louis: Mosby,1994:613-618

4. Chamberlain MC, Sandy AD, Press GA. Leptomeningeal metasta-sis: a comparison of gadolinium-enhanced MR and contrast-en-hanced CT of the brain. Neurology 1990;40:435-438

5. Blews DE, Wang H, Kumer AJ, Robb PA, Phillips PC, et al.Intradural spinal metastases in pediatric patients with primary in-tracranial neoplasms: Gd-DTPA enhanced MR vs CT myelogra-phy. J Comput Assist Tomogr 1990;14:730-735

6. Sze G, Abramson A, Krol G, Liu D, Amster J, Zimmerman RD, etal. Gadolinium-DTPA in the evaluation of intradural-ex-tramedullary spinal disease. AJR Am J Roentgenol 1988;150:911-921

7. Kochi M, Mihara Y, Takada A, Yatomi C, Morioka M, YamashiroS, et al. MRI of subarachnoid dissemination of medulloblastomaNeuroradiology 1991;33:264-268

8. Sze G. Magnetic resonance imaging in the evaluation of spinal tu-mors. Cancer 1991;67:1229-1241

9. Hudgins PA, Davis PC, Hoffman JC Jr. Gadopentetate dimeglu-mine-enhanced MR imaging in children following surgery forbrain tumor: spectrum of meningeal findings. AJNR Am JNeuroradiol 1991;12: 301-307

10. Sze G. Gadolinium-DTPA in spinal disease. Radiol Clin North Am1988;26:1009-1024

11. Paakkao E, Patronas NJ, Schellinger D. Meningeal Gd-DTPA en-hancement in patients with malignancies. J Comput Assist Tomogr1990;14:542-546

12. Sze G. Diseases of intracranial meninges: MR imaging features.AJR Am J Roentgenol 1993;160:727-733

13. River Y, Schwartz A, Gomori JM, Soffer D, Siegel T. Clinical sig-nificance of diffuse dural enhancement detected by magnetic reso-nance imaging. J Neurosurg 1996;85:777-783

14. Henegar MM, Moran CJ, Silbergeld DL. Early postoperative mag-netic resonance imaging following nonneoplastic cortical resec-tion. J Neurosurg 1996;84:174-179

15. Sze G, Soletsky S, Bronen R, Krol G. MR imaging of the cranialmeninges with emphasis on contrast enhancement and meningealcarcinomatosis. AJNR Am J Neuroradiol 1989;10:965-975

16. Gero B, Sze G, Sharif H. MR imaging of intradural inflammatorydiseases of the spine. AJNR Am J Neuroradiol 1991;12:1009-1019

17. Nesbit GM, Miller GM, Baker HL Jr, Ebersold MJ, ScheithauerBW. Spinal cord sarcoidosis: a new finding at MR imaging withGd-DTPA enhancement. Radiology 1989;173:839-843

18. Watanabe M, Tanaka R, Takeda N. Correlation of MRI and clini-cal features in meningeal carcinomatosis. Neuroradiology 1993;35:512-515

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19. Freilich RJ, Krol G, DeAngelis LM. Neuroimaging and cere-brospinal fluid cytology in the diagnosis of leptomeningeal metas-tasis. Ann Neurol 1995;38:51-57

20. Glass JP, Melamed M, Chernick NL, Posner JB. Malignant cells incerebrospinal fluid (CSF): the meaning of a positive CSF cytology.Neurology 1979;29:1369-1375

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대한영상의학회지 2004;51:459-464

자기공명영상에서수아세포종의뇌척수강내조영증강에대한평가1

1서울대학교의과대학방사선과학교실, 서울대학교의학연구원방사선의학연구소

김화영·김인원·김우선·천정은·연경모

목적: 뇌척수강내로의 전이가 흔한 수아세포종이 있는 환자에서 뇌척수강의 조영증강의 유형과 전이와의 상관관계를

분석하고자 한다.

대상과 방법: 25명의 환자에서 수아세포종으로 수술 후에 시행한 84개의 자기공명영상을 후향적으로 분석하였다. 나이

는 2-13 세였고 자기공명영상에서 척수강내의 조영증강 유형을 분석하고 뇌척수액 세포검사에서 전이를 비교확인하

였다. 조영증강은 연뇌막 조영증강에 따라 제 1유형은 세밀하거나 비연속적인 선상 조영증강, 제 2유형은 연속적인 선

상 또는 결절상의 조영증강, 제 3유형은 뇌막내 종괴형성으로 분류하였다. 처음검사와 추적검사에서 자기공명영상에서

의 조영증강유형과 뇌척수액세포검사를 비교하였다.

결과: 총 25명의 환자 중, 제 1유형은 14명에서 관찰되었고 이중 12명은 첫 뇌척수액 세포검사에서 음성이었고 2명은

양성이었다. 추적검사에서 제1유형의 조영증강의 범위에 거의 변화가 없거나 약간 줄어들었고 뇌척수액 세포검사에서

모두 음성이었다. 제 2유형은 7명에서 관찰되었고 첫 뇌척수액 세포검사에서 모두 양성이었다. 추적검사에서 1명을 제

외한 6명의 환자에서 자기공명영상에서 조영증강이 감소되었고 뇌척수액검사에서도 음성으로 바뀌었다. 제 3유형의

조영증강은 4명에서 보였고 첫 뇌척수액검사에서 모두 양성이었다. 추적 MRI에서 모두 조영증강이 증가되었고 뇌척수

액검사도 양성이었다.

결론: 수아세포종으로 진단 후 수술한 환자의 조영증강후 척추 자기공명영상에서 제 2유형과 제 3유형은 전이를 나타

내지만 제 1유형은 전이의 가능성이 낮았다.