Journal of Neuro-Oncology

, Volume 4, Issue 3, pp 243–268 | Cite as

Correlation of neuropathologic findings, computerized tomographic and high-resolution ultrasound scans of canine avian sarcoma virus-induced brain tumors

  • Richard H Brittt
  • Bernard E Lyonsl
  • Dieter R Enzmann
  • Edward L Saxer
  • Sandra H Bigner
  • Darell D. Bigner
Regular Papers

Abstract

The location, size, geometry and neuropathological findings of anaplastic astrocytomas (AA), gliosarcomas and sarcomas induced by the avian sarcoma virus (ASV) in dogs were compared with images generated using computerized tomography (CT) and real time high-resolution ultrasound (HRUS). Seven AA showed a wide range of findings on CT. Pre-contrast CT scans showed that the tumors could be hyper, hypo, or isodense. Three of seven AA had no contrast enhancement; two of these tumors were also isodense which resulted in a false-negative CT exam. Partial enhancement was seen in one tumor. This resulted in a sensitivity of detection of 72%. Real time HRUS was able to define tumor location, size and geometry of the AA missed or incompletely imaged by CT. All tumors were hyperechoic. Inhomogeneity of the echo pattern was due to hemorrhage, cyst formation, and necrosis within the tumors. Such secondary tumor characteristics were more accurately defined by HRUS compared to CT. Vasogenic edema in the brain surrounding tumors was of low density on CT and hypoechoic or indistinguishable from normal brain on US. Similar findings were seen in six gliosarcomas, two of which were not visualized by either pre- or post-contrast enhanced CT scans (sensitivity of 66%). Sarcomas differed in that they were either hyper or isodense; none were hypodense. The area of increased density matched the tumor geometry and correlated with dense cellularity and reticulin deposition. All 13 sarcomas showed contrast enhancement (100% sensitivity), but in two tumors, contrast enhanced CT underestimated the size of the tumor. Because of the large size and multiplicity of the sarcomas, HRUS imaging was not able to resolve the entire tumor volume because of limited imaging access. Intravenously injected horseradish peroxidase (HRP) crossed the tumor blood-brain barrier (BBB) only in those tumors in which contrast enhancement was seen. These studies suggest that intraoperative HRUS imaging may be useful in detecting and delineating human AA incompletely visualized by CT.

Keywords

computerized tomography ultrasound avian sarcoma virus glioblastoma multiforme anaplastic astrocytoma gliosarcoma, sarcoma 

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References

  1. 1.
    Adams JC: Technical considerations on the use of horseradish peroxidase as a neuronal marker. Neuroscience 2:141 - 145, 1977.Google Scholar
  2. 2.
    Afra D, Norman D, Levin VA: Cysts in malignant gliomas. Identification by computerized tomography. J Neurosurg 53:821 - 825, 1980.Google Scholar
  3. 3.
    Ambrose J, Gooding MR, Richardson AE: An assessment of the accuracy of computerized transverse axial scanning (EMI scanner) in the diagnosis of intracranial tumor. A review of 366 patients. Brain 98:569 - 582, 1975.Google Scholar
  4. 4.
    Apuzzo MLJ, Sabshin JK: Computed tomographic guidance stereotaxis in the management of intracranial mass lesions. Neurosurgery 12:277–285, 1983.Google Scholar
  5. 5.
    Baker HL Jr, Houser OW, Campbell JK: National Cancer Institute study: evaluation of computed tomography in the diagnosis of intracranial neoplasms. 1. Overall results. Radiology 136:91–96, 1980.Google Scholar
  6. 6.
    Bergström M, Collins VP, Ehrin E et al: Discrepancies in brain tumor extent as shown by computed tomography and positron emission tomography using (68Ga)EDTA, (11C)glucose, and (11C)methionine. J Comput Assist Tomogr 7:1062–1066, 1983.Google Scholar
  7. 7.
    Bigner DD, Odom GL, Mahaley MS Jr, et al: Brain tumors induced in dogs by the Schmidt-Ruppin strain of Rous sarcoma virus. J Neuropath Exp Neurol 28:648 - 680, 1969.Google Scholar
  8. 8.
    Bigner DD, Kvedar JP, Shaffer TC et al: Factors influencing the cell brain tumors induced in dogs by Schmidt-Ruppin Rous sarcoma virus. J Neuropath Exp Neurol 31:583–595, 1972.Google Scholar
  9. 9.
    Bigner DD, Pegram CN: Virus-induced experimental brain tumors and putative associations of viruses with human brain tumors: a review. Adv Neurol 15:57 - 83, 1976.Google Scholar
  10. 10.
    Blasberg RG, Groothuis D, Molnar P: Application of quantitative autoradiographic measurements in experimental brain tumor models. Sem Neurol 1:203–221, 1981.Google Scholar
  11. 11.
    Boëthius J, Collins VP, Edner G et al: Stereotactic biopsies and computer tomography in gliomas. Acta Neurochir 40:223–232, 1978.Google Scholar
  12. 12.
    Bolender NF, Cromwell LD, Graves V et al: Interval appearance of glioblastomas not evident in previous CT examinations. J Comput Assist Tomogr 7:599–603, 1983.Google Scholar
  13. 13.
    Brady TJ, Buonanno FS, Pykett IL et al: Preliminary clinical results of proton (1H) imaging of cranial neoplasms: in vivo measurements of T1 and mobile proton density. AJNR 4:225–228, 1983.Google Scholar
  14. 14.
    Brant-Zawadski M, Badami JP, Mills CM et al: Primary intracranial tumor imaging with magnetic resonance: a comparison of magnetic resonance and CT. Radiology 150:435 - 440, 1984.Google Scholar
  15. 15.
    Brightman MW: The intracerebral movement of proteins injected into blood and cerebrospinal fluid of mice. Progr Brain Res 29:19–37, 1968.Google Scholar
  16. 16.
    Brightman MW, Reese TS: Junction between intimitely apposed cell membranes in the vertebrate brain. J Cell Biol 40:648–677, 1969.Google Scholar
  17. 17.
    Brightman MW, Reese TS, Vick NA et al: A mechanism underlying the lack of a blood-brain barrier to peroxidase in virally induced brain tumors (Abstract). J Neuropath Exp Neurol 30:139- 140, 1971.Google Scholar
  18. 18.
    Britt RH, Lyons B, Pounds D et al: Feasibility of using ultrasound hyperthermia in the treatment of malignant brain tumors: Tissue damage threshold and thermal dosimetry studies. Med Instrument 17:172–177, 1983.Google Scholar
  19. 19.
    Britt RH, Pounds DW, Lyons BE: Feasibility of treating malignant brain tumors with focused ultrasound. In: Rosenblum ML, Wilson CB (eds): Progress in Experimental Brain Tumor Research. II. Brain Tumor Therapy. S Karger, Basel, 1984, pp 232–245.Google Scholar
  20. 20.
    Britt RH, Lyons BE, Eng LF et al: Immunohistochemical study of glial fibrillary acidic protein in Avian sarcoma virus induced gliomas in dogs. J Neuro-Oncol 3:53 - 59, 1985.Google Scholar
  21. 21.
    Bucciarelli E, Rabotti GF, Dalton AJ: Ultrastructure of gliomas induced in hamsters with Rous sarcoma virus. J Natl Cancer Inst 38:865 - 889, 1967.Google Scholar
  22. 22.
    Buonanno FS, Pykett IL, Brady TJ et al: Clinical relevance of two different nuclear magnetic resonance (NMR) approaches to imaging of a low grade astrocytoma. J Comput Assist Tomogr 6:529–535, 1982.Google Scholar
  23. 23.
    Burger PC, Bigner DD, Self DJ: Morphological observations of brain tumors in PD4 hamsters induced by four strains of Avian sarcoma virus. Acta Neuropath (Berl) 26:1- 21, 1973.Google Scholar
  24. 24.
    Burger PC, Dubois PJ, Schold SC Jr et al: Computerized tomographic and pathologic studies of the untreated, quiescent and recurrent glioblastoma multiforme. J Neurosurg 58:159 - 169, 1983.Google Scholar
  25. 25.
    Butler AR, Horii SC, Kricheff II et al: Computed tomography in astrocytomas. A statistical analysis of the parameters of malignancy and the positive contrastenhanced CT scan. Radiology 129:433–439, 1978.Google Scholar
  26. 26.
    Bydder GM, Steiner RE, Young IR et al: Clinical NMR imaging of the brain: 140 cases. AJNR 3:459–480, 1982.Google Scholar
  27. 27.
    Chandler WF, Knake JE, McGillicuddy JE et al: Intraoperative use of real-time ultrasonography in neurosurgery. J Neurosurg 57:157–163, 1982.Google Scholar
  28. 28.
    Copeland DD, Talley FA, Bigner DD: The fine structure of intracranial neoplasms induced by the inoculation of Avian sarcoma virus in neonatal and adult rats. Am J Pathol 83:149–176, 1976.Google Scholar
  29. 29.
    Cox D, Pilkington G, Lantos P: The fine structure of blood vessels in ENU induced tumours of the rat nervous system. With special references to the breakdown of the blood-brain barrier. Br J Exp Path 57:419–430, 1976.Google Scholar
  30. 30.
    Deane BR, Lantos PL: The vasculature of experimental brain tumours, Part 2 (a quantitative assessment of morphological abnormalities). J Neurol Sci 49:67–77, 1981.Google Scholar
  31. 31.
    Dewbury KC, Bates RI: Neonatal intracranial haemorrhage: the casue of the ultrasound appearances. Br J Radiol 56:783 - 789, 1983.Google Scholar
  32. 32.
    Dohrmann GJ, Rubin JM: Use of ultrasound in neurosurgical operations: a preliminary report. Surg Neurol 16:362 - 366, 1981.Google Scholar
  33. 33.
    Enzmann DR, Britt RH, Lyons B et al: Experimental study of high-resolution ultrasound imaging of hemorrhage, bone fragments, and foreign bodies in head trauma. J Neurosurg 54:304- 309, 1981.Google Scholar
  34. 34.
    Enzmann DR, Britt RH, Lyons BE et al: Natural history of experimental intracerebral hemorrhage: sonography, computed tomography and neuropathology. AJNR 2:517–526, 1981.Google Scholar
  35. 35.
    Enzmann DR, Britt RH, Lyons B et al: High-resolution ultrasound evaluation of experimental brain abscess evolution: comparisons with computed tomography and neuropathology. Radiology 142:95–102, 1982.Google Scholar
  36. 33.
    Enzmann DR, Murphy-Irwin K, Fine M et al: Intraoperative and outpatient echoencephalography through a burr hole. Neuroradiology 26:57–60, 1984.Google Scholar
  37. 37.
    Enzmann DR, Murphy-Irwin K, Marshall WH et al: Intraoperative sonography through a burr hole. AJNR 5:243–246, 1984.Google Scholar
  38. 38.
    Enzmann DR, Wheat R, Marshall WH et al: Tumors of the central nervous system studied by computed tomography and ultrasound. Radiology 154:393–399, 1985.Google Scholar
  39. 39.
    Fields S, Dunn F: Correlation of echogenic visualizability of tissue with biological composition and physiological state. J Acoust Soc Am 54:809–812, 1973.Google Scholar
  40. 40.
    Fike JR, LeCouteur RA, Cann CE et al: Computerized tomography of brain tumors of the rostral and middle fossas in the dog. Am J Vet Res 42:275–281, 1981.Google Scholar
  41. 41.
    Gado MH, Phelps MD, Coleman RE: An extravascular component of contrast enhancement in cranial computed tomography. Radiology 117:589–593, 1975.Google Scholar
  42. 42.
    Gooding GAW, Boggan JE, Bank WO et al: Sonography of the adult brain through surgical defects. AJNR 2:449–452, 1981.Google Scholar
  43. 43.
    Gooding GAW, Edwards MSB, Rabkin AE et al: Intraoperative real-time ultrasound in the localization of intracranial neoplasms. Radiology 146:459–462, 1983.Google Scholar
  44. 44.
    Greenleaf JF: Three-dimensional imaging in ultrasound. J Med Syst 6:579–597, 1982.Google Scholar
  45. 45.
    Groothuis DR, Fischer JM, Vick NA et al: Comparative permeability of different glioma models to horseradish peroxidase. Cancer Treat Rep 65 (Suppl 2):13–18, 1981.Google Scholar
  46. 46.
    Groothuis DR, Mikhael MA, Fischer JM et al: Computed tomography of virally induced canine brain tumors: a preliminary report. J Comput Assist Tomogr 5:538–543, 1981.Google Scholar
  47. 47.
    Groothuis DR, Fischer JM, Lapin G et al: Permeability of different experimental brain tumor models to horseradish peroxidase. J Neuropath Exp Neurol 41:164–185, 1982.Google Scholar
  48. 48.
    Groothuis DR, Vick NA: Brain tumors and the bloodbrain barrier. Trends Neurosci 5:232–234, 1982.Google Scholar
  49. 49.
    Gutin PH, Phillips TL, Wara WM et al: Brachytherapy of recurrent malignant brain tumors with removable highactivity iodine-125 sources. J Neurosurg 60:61–68, 1984.Google Scholar
  50. 50.
    Hawkes RC, Holland GN, Moore WS et al: NMR tissue characterization in intracranial tumors: preliminary results. AJNR 4:830–832, 1983.Google Scholar
  51. 51.
    Hirano A, Zimmerman H: Fenestrated blood vessels in a metastatic renal carcinoma in the brain. Lab Invest 26:465–468, 1972.Google Scholar
  52. 52.
    Hirano A, Matsui T: Vascular structures in brain tumors. Human Path 6:611–621, 1975.Google Scholar
  53. 53.
    Hochberg FH, Pruitt A: Assumptions in the radiotherapy of glioblastoma. Neurology 30:907–911, 1980.Google Scholar
  54. 54.
    Hossmann KA, Bothe HW, Bodsch W et al: Pathophysiological aspects of blood-brain barrier disturbances in experimental brain tumors and brain abscesses. Acta Neuropathol (Berl) 8 (Suppl):89–102, 1983.Google Scholar
  55. 55.
    Hurter T, Brocker W, Hossman KA: Evaluation of vasogenic edema in experimental brain tumors by cathodoluminescence and fluorescence microscopy. Histochemistry 72:249–254, 1981.Google Scholar
  56. 56.
    Jacobs L, Kinkel WR, Heffner RR Jr: Autopsy correlations of computerized tomography: experience with 6000 CT scans. Neurology 26:1111–1118, 1976.Google Scholar
  57. 57.
    Jacques S, Sheldon CH, McCann GD et al: Computerized three-dimensional stereotaxic removal of small central nervous system lesions in patients. J Neurosurg 53:816–820, 1980.Google Scholar
  58. 58.
    Jezernik M, Sentjurc M, Schara M: Proton magnetic resonance characterization of brain tumors. Acta Neurochir 67:1–9, 1983.Google Scholar
  59. 59.
    Kapp JP, Holla PS: Detection of experimental brain tumor in rat by computed tomography. Surg Neurol 16:455–458, 1981.Google Scholar
  60. 60.
    Kelly PJ, Alker GJ Jr, Goerss S: Computer-assisted stereotactic laser microsurgery for the treatment of intracranial neoplasms. Neurosurgery 10:324–331, 1982.Google Scholar
  61. 61.
    Kelly PJ, Kall B, Goerss S et al: Precision resection of intra-axial CNS lesions by CT-based stereotactic craniotomy and computer monitored CO2 laser. Acta Neurochir 68:1–9, 1983.Google Scholar
  62. 62.
    Kricheff II, Lin JP, Pay N: Some aspects of the computed tomography of the head. Natl Cancer Inst Monogr 46:109–117, 1977.Google Scholar
  63. 63.
    Kristler JP, Hochberg FH, Brooks BR et al: Computerized axial tomography: clinicopathologic correlation. Neurology 25:201–209, 1975.Google Scholar
  64. 64.
    Kurtz AB, Dubbins PA, Rubin CS et al: Echogenicity: analysis, significance, and masking. AJR 137:471–476, 1981.Google Scholar
  65. 65.
    Latchaw RE, Gold LHA, Moore JS Jr et al: The nonspecificity of absorption coefficients in the differentiation of solid tumors and cystic lesions. Radiology 125:141–144, 1977.Google Scholar
  66. 66.
    LeCouteur RA, Fike JR, Cann CE et al: Computed tomography of brain tumors in the caudal fossa of the dog. Am Coll Vet Radiol 22:244–251, 1981.Google Scholar
  67. 67.
    Leksell L. Stereotactic radiosurgery. J Neurol Neurosurg Psychiat 46:797–803, 1983.Google Scholar
  68. 68.
    Lewander R: Contrast enhancement with time in gliomas. Stereotactic computer tomography following contrast medium infusion. Acta Radiolog Diag 20:689–702, 1979.Google Scholar
  69. 69.
    Lillehei KO, Chandler WF, Knake JE: Real time ultrasound characteristics of the acute intracerebral hemorrhage as studied in the canine model. Neurosurgery 14:48–51, 1984.Google Scholar
  70. 70.
    Long DM: Capillary ultrastructure and the blood-brain barrier in human malignant brain tumors. J Neurosurg 32:127–144, 1970.Google Scholar
  71. 71.
    Lyons BE, Britt RH, Strohbehn JW: Localized hyperthermia in the treatment of malignant brain tumors using an interstitial microwave antenna array. IEEE Trans Biomed Engineer 31:53–62, 1984.Google Scholar
  72. 72.
    Marks JE, Gado M: Serial computed tomography of primary brain tumors following surgery, irradiation, and chemotherapy. Radiology 125:119–125, 1977.Google Scholar
  73. 73.
    Matsui T: Neuropathological studies of CT findings in glioblastoma multiforme (Abstract). J Comput Assist Tomogr 3:566, 1979.Google Scholar
  74. 74.
    McCullough DC, Huang HK, DeMichelle D et al: Correlation between volumetric CT imaging and autopsy measurements of glioblastoma size. Comput Tomogr 3:133–141, 1979.Google Scholar
  75. 75.
    Mundinger F, Ostertag CB, Birg W et al: Stereotactic treatment of drug lesions. Biopsy, interstitial radiotherapy (Iridium-192 and Iodine-125) and drainage procedures. Appl Neurophysiol 43:198–204, 1980.Google Scholar
  76. 76.
    Neuwelt EA, Barnett PA, Frenkel EF: Chemotherapeutic agent permeability to normal brain and delivery to Aviam sarcoma virus-induced brain tumors in the rodent: observations on problems of drug delivery. Neurosurgery 14:154–160, 1984.Google Scholar
  77. 77.
    Norman D, Enzmann DR, Levin VA et al: Computed tomography in the evaluation of malignant glioma before and after therapy. Radiology 121:85–88, 1976.Google Scholar
  78. 78.
    Nyström S: Pathological changes in blood vessels of human glioblastoma multiforme. Comparative studies using plastic casting, angiography, light microscopy, and electron microscopy, and with reference to some other brain tumors. Acta Path Microbiol Scand 49 (Suppl 137):1–85, 1960.Google Scholar
  79. 79.
    Ostertag CB, Mennel HD, Kiessling M: Stereotactic biopsy of brain tumors. Surg Neurol 14:275–283, 1980.Google Scholar
  80. 80.
    Patrick JT, Fry FJ, Gardner G et al: Ultrasound tomography of excised brains: normal and pathological anatomy. In: White D, Lyons EA (eds): Ultrasound in Medicine, Vol 4. Plenum Publishing Corporation, New York, 1978, pp 269–276.Google Scholar
  81. 81.
    Price RR, Jones TB, Goddard J et al: Basic concepts of ultrasonic tissue characterization. Radiol Clin N Am 18:21–30, 1980.Google Scholar
  82. 82.
    Rabotti GF, Grove AS, Sellers RL et al: Induction of multiple brain tumours (gliomata and leptomeningeal sarcomata) in dogs by Rous sarcoma virus. Nature 209:884–886, 1966.Google Scholar
  83. 83.
    Reese TS, Karnovsky MJ: Fine structural localization of blood-brain barrier to exogenous peroxidase. J Cell Biol 37:207–217, 1967.Google Scholar
  84. 84.
    Rieth KG, Di Chiro G, London WT et al: Experimental glioma in primates: a computed tomography model. J Comput Assist Tomogr 4:285–290, 1980.Google Scholar
  85. 85.
    Roberts DW, Coughlin CT, Wong TZ et al: Interstitial microwave hyperthermia and iridium brachytherapy in the treatment of malignant gliomas: A Phase I clinical trial. J Neurosurg 18:581–587, 1986.Google Scholar
  86. 86.
    Rubin JM, Mirfakhraee M, Duda EE et al: Intraoperative ultrasound examination of the brain. Radiology 137:831–832, 1980.Google Scholar
  87. 87.
    Rubin JM, Dohrmann GJ, Greenberg M et al: Intraoperative sonography on meningiomas. AJNR 3:305–308, 1982.Google Scholar
  88. 88.
    Rubin JM, Dohrmann GJ: Use of ultrasonically guided probes and catheters in neurosurgery. Surg Neurol 18:143–148, 1982.Google Scholar
  89. 89.
    Rubin JM, Dohrmann GJ: Intraoperative neurosurgical ultrasound in the localization and characterization of intracranial masses. Radiology 148:519–524, 1983.Google Scholar
  90. 90.
    Salcman M, Levine H, Rao K: Value of sequential computed tomography in the multimodality treatment of glioblastoma multiforme. Neurosurgery 8:15–19, 1981.Google Scholar
  91. 91.
    Salcman M, Samaras GM: Interstitial microwave hyperthermia for brain tumors. J Neuro-Oncol 1:225–236, 1983.Google Scholar
  92. 92.
    Shalit MN, Israeli Y, Matz S et al: Experience with intraoperative CT scanning in brain tumors. Surg Neurol 17:376–382, 1982.Google Scholar
  93. 93.
    Sheldon CH, McCann G, Jacques S et al: Development of a computerized microstereotaxic method for localization and removal of minute CNS lesions under direct 3-D vision. J Neurosurg 52:21–27, 1980.Google Scholar
  94. 94.
    Silberman AW, Morton DF, Storm FK et al: Combination radiofrequency hyperthermia and chemotherapy (BCNU) for brain malignancy. J Neuro-Oncol 2:19–28, 1984.Google Scholar
  95. 95.
    Sipe JC, Vick NA, Bigner DD: Grey matter edema: the marginal zone of autochtonous virally-induced gliomas. J Neurol Sci 17:185–191, 1972.Google Scholar
  96. 96.
    Tanaka K, Ito K, Wagai T: The localization of brain tumors by ultrasonic techniques. J Neurosurg 23:135–147, 1965.Google Scholar
  97. 97.
    Tentler RL, Palacios E: False-negative computerized tomography in brain tumor. JAMA 238:339–340, 1977.Google Scholar
  98. 98.
    Thompson JLG: Computerized axial tomography and diagnosis of glioma: a study of 100 consecutive histologically proven cases. Clin Radiol 27:431–441, 1976.Google Scholar
  99. 99.
    Tsutsumi Y, Andoh Y, Inoue N: Ultrasound-guided biopsy for deep-seated brain tumors. J Neurosurg 57:164–167, 1982.Google Scholar
  100. 100.
    van Venrooij GEPM, Boone RM, van der Gon JJD: Two-dimensional echo-encephalography: 1. Acoustic properties of some tissues and the characteristics of echo patterns obtained using equipment especially adapted for detection of these tissues. Acta Neurochir (Wien) 49:1–8, 1979.Google Scholar
  101. 101.
    Vick NA, Bigner DD, Kvedar JP: The fine structure of canine gliomas and intracranial sarcomas induced by the Schmidt-Ruppin strain of the Rous sarcoma virus. J Neuropath Exp Neurol 30:354–367, 1971.Google Scholar
  102. 102.
    Vick NA, Bigner DD: Some structural aspects of dog brain tumors induced with Schmidt-Ruppin strain of Rous sarcoma virus. Prog Exp Tumor Res 17:59–73, 1972.Google Scholar
  103. 103.
    Vick NA, Bigner DD: Microvasculature abnormalities in virally induced canine brain tumors: structural bases for altered blood-brain barrier function. J Neurol Sci 17:29–39, 1972.Google Scholar
  104. 104.
    Vick NA: Brain tumor microvasculature. In: Weiss L, Gilbert HA, Posner JB (eds): Brain Metastasis. GK Hall, New York, 1980, pp 115–133.Google Scholar
  105. 105.
    Volc D, Jellinger K, Flament H et al: Cerebral space-occupying cysts following radiation and chemotherapy of malignant gliomas. Acta Neurochir 57:177–193, 1981.Google Scholar
  106. 106.
    Weller R, Fox M, Cox S: The development and ultrastructure of the microvasculature in malignant gliomas. Neuropath Appl Neurobiol 3:307–322, 1977.Google Scholar
  107. 107.
    Wilfong RF, Bigner DD, Self DJ et al: Brain tumor types induced by Schmidt-Ruppin strain of Rous sarcoma virus in inbred Fischer rats. Acta Neuropath (Berl) 25:196–206, 1973.Google Scholar
  108. 108.
    Zimmerman RA, Bilaniuk LT, Goldberg HI et al: Cerebral NMR imaging: early results with a.12T resistive system. AJR 141:1187–1194, 1983.Google Scholar

Copyright information

© Martinus Nijhoff Publishers 1987

Authors and Affiliations

  • Richard H Brittt
    • 1
    • 2
  • Bernard E Lyonsl
    • 2
  • Dieter R Enzmann
    • 3
    • 4
  • Edward L Saxer
    • 1
    • 2
  • Sandra H Bigner
    • 5
  • Darell D. Bigner
    • 5
  1. 1.Department of SurgeryStanford University Medical CenterStanfordUSA
  2. 2.Department Division of NeurosurgeryStanford University Medical CenterStanfordUSA
  3. 3.Department of RadiologyStanford University Medical CenterStanfordUSA
  4. 4.Division of NeuroradiologyStanford University Medical CenterStanfordUSA
  5. 5.Department of PathologyDuke University Medical CenterDurhamUSA

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