Seminars in Oncology
Volume 31, Issue 5 , Pages 702-713 , October 2004

Cognitive sequelae of brain radiation in adults

  • Nadia N. Laack

      Affiliations

    • Division of Radiation Oncology, Mayo Clinic, Rochester, MN, USA.
  • ,
  • Paul D. Brown

      Affiliations

    • Division of Radiation Oncology, Mayo Clinic, Rochester, MN, USA.
    • Corresponding Author InformationAddress reprint requests to Paul D. Brown, MD, 200 First St SW, Rochester, MN 55905.

References 

  1. Reijneveld JC , Sitskoorn MM , Klein M , et al.   Cognitive status and quality of life in patients with suspected versus proven low-grade gliomas . Neurology . 2001;56:618–623
  2. Schultheiss TE , Kun LE , Ang KK , et al.   Radiation response of the central nervous system . Int J Radiat Oncol Biol Phys . 1995;31:1093–1112
  3. O’Brien P , Roos D , Pratt G , et al.   Phase II multicenter study of brief single-agent methotrexate followed by irradiation in primary CNS lymphoma . J Clin Oncol . 2000;18:519–526
  4. Torres IJ , Mundt AJ , Sweeney PJ , et al.   A longitudinal neuropsychological study of partial brain radiation in adults with brain tumors . Neurology . 2003;60:1113–1118
  5. Taylor BV , Buckner JC , Cascino TL , et al.   Effects of radiation and chemotherapy on cognitive function in patients with high-grade glioma . J Clin Oncol . 1998;16:2195–2201
  6. Klein M , Heimans JJ , Aaronson NK , et al.   Effect of radiotherapy and other treatment-related factors on mid-term to long-term cognitive sequelae in low-grade gliomas (A comparative study) . Lancet . 2002;360:1361–1368
  7. Dropcho EJ . Central nervous system injury by therapeutic irradiation . Neurol Clin . 1991;9:969–988
  8. Tofilon PJ , Fike JR . The radioresponse of the central nervous system (A dynamic process) . Radiat Res . 2000;153:357–370
  9. Kramer S . The hazards of therapeutic iradiation of the central nervous system . Clin Neurosurg . 1968;15:301–318
  10. Hopewell JW , Wright EA . The nature of latent cerebral irradiation damage and its modification by hypertension . Br J Radiol . 1970;43:161–167
  11. Sheline GE , Wara WM , Smith V . Therapeutic irradiation and brain injury . Int J Radiat Oncol Biol Phys . 1980;6:1215–1228
  12. van der Kogel AJ . Radiation-induced damage in the central nervous system (An interpretation of target cell responses) . Br J Cancer . 1986;7(suppl):207–217
  13. Belka C , Budach W , Kortmann RD , et al.   Radiation induced CNS toxicity—Molecular and cellular mechanisms . Br J Cancer . 2001;85:1233–1239
  14. Nieder C , Andratschke N , Price RE , et al.   Innovative prevention strategies for radiation necrosis of the central nervous system . Anticancer Res . 2002;22:1017–1023
  15. Boldrey E , Sheline G . Delayed transitory clinical manifestation after radiation treatment of intracranial tumors . Acta Radiol . 1967;5:5–10
  16. Di Chiro G , Oldfield E , Wright DC , et al.   Cerebral necrosis after radiotherapy and/or intraarterial chemotherapy for brain tumors (PET and neuropathologic studies) . AJR Am J Roentgenol . 1988;150:189–197
  17. Schlemmer HP , Bachert P , Henze M , et al.   Differentiation of radiation necrosis from tumor progression using proton magnetic resonance spectroscopy . Neuroradiology . 2002;44:216–222
  18. Price RA , Jamieson PA . The central nervous system in childhood leukemia. II. Subacute leukoencephalopathy . Cancer . 1975;35:306–318
  19. Emami B , Lyman J , Brown A , et al.   Tolerance of normal tissue to therapeutic irradiation . Int J Radiat Oncol Biol Phys . 1991;21:109–122
  20. Shaw E . Central nervous system tumors (Overview) . In:  Gunderson LL ,  Tepper JE editor. Clinical Radiation Oncology . Philadelphia, PA: Churchill Livingstone; 2000;p. 314–335
  21. Yang GY , Matthews RH . Prophylactic cranial irradiation in small-cell lung cancer . Oncologist . 2000;5:293–298
  22. Auperin A , Arriagada R , Pignon JP , et al.   Prophylactic cranial irradiation for patients with small-cell lung cancer in complete remission. Prophylactic Cranial Irradiation Overview Collaborative Group . N Engl J Med . 1999;341:476–484
  23. Johnson BE , Patronas N , Hayes W , et al.   Neurologic, computed cranial tomographic, and magnetic resonance imaging abnormalities in patients with small-cell lung cancer (Further follow-up of 6- to 13-year survivors) . J Clin Oncol . 1990;8:48–56
  24. Fleck JF , Einhorn LH , Lauer RC , et al.   Is prophylactic cranial irradiation indicated in small-cell lung cancer? . J Clin Oncol . 1990;8:209–214
  25. Lee JS , Umsawasdi T , Lee YY , et al.   Neurotoxicity in long-term survivors of small cell lung cancer . Int J Radiat Oncol Biol Phys . 1986;12:313–321
  26. Frytak S , Shaw JN , O’Neill BP , et al.   Leukoencephalopathy in small cell lung cancer patients receiving prophylactic cranial irradiation . Am J Clin Oncol . 1989;12:27–33
  27. Komaki R , Meyers CA , Shin DM , et al.   Evaluation of cognitive function in patients with limited small cell lung cancer prior to and shortly following prophylactic cranial irradiation . Int J Radiat Oncol Biol Phys . 1995;33:179–182
  28. van Oosterhout AG , Boon PJ , Houx PJ , et al.   Follow-up of cognitive functioning in patients with small cell lung cancer . Int J Radiat Oncol Biol Phys . 1995;31:911–914
  29. Arriagada R , Le Chevalier T , Borie F , et al.   Prophylactic cranial irradiation for patients with small-cell lung cancer in complete remission . J Natl Cancer Inst . 1995;87:183–190
  30. Gregor A , Cull A , Stephens RJ , et al.   Prophylactic cranial irradiation is indicated following complete response to induction therapy in small cell lung cancer: Results of a multicentre randomised trial. United Kingdom Coordinating Committee for Cancer Research (UKCCCR) and the European Organization for Research and Treatment of Cancer (EORTC) . Eur J Cancer . 1997;33:1752–1758
  31. Parageorgiou C , Dardoufas C , Kouloulias V , et al.   Psychophysiological evaluation of short-term neurotoxicity after prophylactic brain irradiation in patients with small cell lung cancer (A study of event related potentials) . J Neurooncol . 2000;50:275–285
  32. DeAngelis LM , Delattre JY , Posner JB . Radiation-induced dementia in patients cured of brain metastases . Neurology . 1989;39:789–796
  33. Klein M , Taphoorn MJ , Heimans JJ , et al.   Neurobehavioral status and health-related quality of life in newly diagnosed high-grade glioma patients . J Clin Oncol . 2001;19:4037–4047
  34. Smalley SR , Laws ER , O’Fallon JR , et al.   Resection for solitary brain metastasis. Role of adjuvant radiation and prognostic variables in 229 patients . J Neurosurg . 1992;77:531–540
  35. Kelly K , Bunn PA . Is it time to reevaluate our approach to the treatment of brain metastases in patients with non-small cell lung cancer? . Lung Cancer . 1998;20:85–91
  36. Penitzka S , Steinvorth S , Sehlleier S , et al.   Assessment of cognitive function after preventive and therapeutic whole brain irradiation using neuropsychological testing . Strahlenther Onkol . 2002;178:252–258
  37. Regine WF , Scott C , Murray K , et al.   Neurocognitive outcome in brain metastases patients treated with accelerated-fractionation vs. accelerated-hyperfractionated radiotherapy (An analysis from Radiation Therapy Oncology Group Study 91–04) . Int J Radiat Oncol Biol Phys . 2001;51:711–717
  38. Stewart LA . Chemotherapy in adult high-grade glioma (A systematic review and meta-analysis of individual patient data from 12 randomised trials) . Lancet . 2002;359:1011–1018
  39. Randomized trial of procarbazine, lomustine, and vincristine in the adjuvant treatment of high-grade astrocytoma. A Medical Research Council trial . J Clin Oncol . 2001;19:509–518
  40. Walker MD , Alexander E , Hunt WE , et al.   Evaluation of BCNU and/or radiotherapy in the treatment of anaplastic gliomas. A cooperative clinical trial . J Neurosurg . 1978;49:333–343
  41. Kristiansen K , Hagen S , Kollevold T , et al.   Combined modality therapy of operated astrocytomas grade III and IV. Confirmation of the value of postoperative irradiation and lack of potentiation of bleomycin on survival time: A prospective multicenter trial of the Scandinavian Glioblastoma Study Group . Cancer . 1981;47:649–652
  42. Hochberg FH , Slotnick B . Neuropsychologic impairment in astrocytoma survivors . Neurology . 1980;30:172–177
  43. Archibald YM , Lunn D , Ruttan LA , et al.   Cognitive functioning in long-term survivors of high-grade glioma . J Neurosurg . 1994;80:247–253
  44. Trojanowski T , Peszynski J , Turowski K , et al.   Quality of survival of patients with brain gliomas treated with postoperative CCNU and radiation therapy . J Neurosurg . 1989;70:18–23
  45. Westergaard L , Gjerris F , Klinken L . Prognostic parameters in benign astrocytomas . Acta Neurochir . 1993;123:1–7
  46. Janny P , Cure H , Mohr M , et al.   Low grade supratentorial astrocytomas. Management and prognostic factors . Cancer . 1994;73:1937–1945
  47. Philippon JH , Clemenceau SH , Fauchon FH , et al.   Supratentorial low-grade astrocytomas in adults . Neurosurgery . 1993;32:554–559
  48. Piepmeier JM . Observations on the current treatment of low-grade astrocytic tumors of the cerebral hemispheres . J Neurosurg . 1987;67:177–181
  49. Shaw EG , Daumas-Duport C , Scheithauer BW , et al.   Radiation therapy in the management of low-grade supratentorial astrocytomas . J Neurosurg . 1989;70:853–861
  50. Shibamoto Y , Kitakabu Y , Takahashi M , et al.   Supratentorial low-grade astrocytoma. Correlation of computed tomography findings with effect of radiation therapy and prognostic variables . Cancer . 1993;72:190–195
  51. Leighton C , Cairncross G . Low-grade glioma—The Europeans are winning! . J Clin Oncol . 1997;15:2761
  52. Nicolato A , Gerosa MA , Fina P , et al.   Prognostic factors in low-grade supratentorial astrocytomas (A uni-multivariate statistical analysis in 76 surgically treated adult patients) . Surg Neurol . 1995;44:208–221
  53. Piepmeier J , Christopher S , Spencer D , et al.   Variations in the natural history and survival of patients with supratentorial low-grade astrocytomas . Neurosurgery . 1996;38:872–878
  54. Bahary JP , Villemure JG , Choi S , et al.   Low-grade pure and mixed cerebral astrocytomas treated in the CT scan era . J Neurooncol . 1996;27:173–177
  55. Marks JE , Baglan RJ , Prassad SC , et al.   Cerebral radionecrosis (Incidence and risk in relation to dose, time, fractionation and volume) . Int J Radiat Oncol Biol Phys . 1981;7:243–252
  56. Kramer S , Southard ME , Mansfield CM . Radiation effect and tolerance of the central nervous system . Front Radiat Ther Oncol . 1972;6:332–345
  57. Gregor A , Cull A , Traynor E , et al.   Neuropsychometric evaluation of long-term survivors of adult brain tumours (Relationship with tumour and treatment parameters) . Radiother Oncol . 1996;41:55–59
  58. Surma-aho O , Niemela M , Vilkki J , et al.   Adverse long-term effects of brain radiotherapy in adult low-grade glioma patients . Neurology . 2001;56:1285–1290
  59. Asai A , Matsutani M , Takakura K . Subacute brain atrophy induced by radiation therapy of malignant brain tumors . Jpn J Cancer Clin . 1987;33:753–761
  60. Asai A , Matsutani M , Kohno T , et al.   Subacute brain atrophy after radiation therapy for malignant brain tumor . Cancer . 1989;63:1962–1974
  61. Taphoorn MJ , Schiphorst AK , Snoek FJ , et al.   Cognitive functions and quality of life in patients with low-grade gliomas (The impact of radiotherapy) . Ann Neurol . 1994;36:48–54
  62. Kiebert GM , Curran D , Aaronson NK , et al.   Quality of life after radiation therapy of cerebral low-grade gliomas of the adult: Results of a randomised phase III trial on dose response (EORTC trial 22844). EORTC Radiotherapy Co-operative Group . Eur J Cancer . 1998;34:1902–1909
  63. Shaw E , Arusell R , Scheithauer B , et al.   Prospective randomized trial of low- versus high-dose radiation therapy in adults with supratentorial low-grade glioma (Initial report of a North Central Cancer Treatment Group/Radiation Therapy Oncology Group/Eastern Cooperative Oncology Group study) . J Clin Oncol . 2002;20:2267–2276
  64. Brown P , Buckner J , O’Fallon J , et al.   Effects of radiotherapy on cognitive function in patients with low-grade glioma measured by the Folstein Mini-Mental State Examination . J Clin Oncol . 2003;21:2519–2524
  65. Laack N, Brown PD, Furth A, et al: Neurocognitive function after radiotherapy (RT) for supratentorial low-grade gliomas (LGG): Results of a North Central Cancer Treatment Group (NCCTG) prospective study. Abstract presented at the ASTRO, Salt Lake City, UT, October 19–23, 2003
  66. Armstrong CL , Corn BW , Ruffer JE , et al.   Radiotherapeutic effects on brain function (double dissociation of memory systems) . Neuropsychiatry Neuropsychol Behav Neurol . 2000;13:101–111
  67. Armstrong CL , Hunter JV , Ledakis GE , et al.   Late cognitive and radiographic changes related to radiotherapy (Initial prospective findings) . Neurology . 2002;59:40–48
  68. Vigliani MC , Sichez N , Poisson M , et al.   A prospective study of cognitive functions following conventional radiotherapy for supratentorial gliomas in young adults (4-year results) . Int J Radiat Oncol Biol Phys . 1996;35:527–533
  69. Nelson DF , Martz KL , Bonner H , et al.   Non-Hodgkin’s lymphoma of the brain: Can high dose, large volume radiation therapy improve survival? Report on a prospective trial by the Radiation Therapy Oncology Group (RTOG): RTOG 8315 . Int J Radiat Oncol Biol Phys . 1992;23:9–17
  70. Herrlinger U , Schabet M , Brugger W , et al.   Primary central nervous system lymphoma 1991–1997 (Outcome and late adverse effects after combined modality treatment) . Cancer . 2001;91:130–135
  71. Bessell EM , Graus F , Lopez-Guillermo A , et al.   CHOD/BVAM regimen plus radiotherapy in patients with primary CNS non-Hodgkin’s lymphoma . Int J Radiat Oncol Biol Phys . 2001;50:457–464
  72. DeAngelis LM , Seiferheld W , Schold SC , et al.   Combination chemotherapy and radiotherapy for primary central nervous system lymphoma (Radiation Therapy Oncology Group study 93–10) . J Clin Oncol . 2002;20:4643–4648
  73. Keime-Guibert F , Napolitano M , Delattre JY . Neurological complications of radiotherapy and chemotherapy . J Neurol . 1998;245:695–708
  74. Basso U , Brandes AA . Diagnostic advances and new trends for the treatment of primary central nervous system lymphoma . Eur J Cancer . 2002;38:1298–1312
  75. Rubin P , Gash DM , Hansen JT , et al.   Disruption of the blood-brain barrier as the primary effect of CNS irradiation . Radiother Oncol . 1994;31:51–60
  76. Blay JY , Conroy T , Chevreau C , et al.   High-dose methotrexate for the treatment of primary cerebral lymphomas (analysis of survival and late neurologic toxicity in a retrospective series) . J Clin Oncol . 1998;16:864–871
  77. Steinvorth S , Wenz F , Wildermuth S , et al.   Cognitive function in patients with cerebral arteriovenous malformations after radiosurgery (Prospective long-term follow-up) . Int J Radiat Oncol Biol Phys . 2002;54:1430–1437
  78. Pirzkall A , Debus J , Lohr F , et al.   Radiosurgery alone or in combination with whole-brain radiotherapy for brain metastases . J Clin Oncol . 1998;16:3563–3569
  79. Sneed PK , Lamborn KR , Forstner JM , et al.   Radiosurgery for brain metastases (Is whole brain radiotherapy necessary?) . Int J Radiat Oncol Biol Phys . 1999;43:549–558
  80. Chidel MA , Suh JH , Reddy CA , et al.   Application of recursive partitioning analysis and evaluation of the use of whole brain radiation among patients treated with stereotactic radiosurgery for newly diagnosed brain metastases . Int J Radiat Oncol Biol Phys . 2000;47:993–999
  81. Yamamoto M , Ide M , Nishio S , et al.   Gamma knife radiosurgery for numerous brain metastases (Is this a safe treatment?) . Int J Radiat Oncol Biol Phys . 2002;53:1279–1283
  82. Regine WF , Huhn JL , Patchell RA , et al.   Risk of symptomatic brain tumor recurrence and neurologic deficit after radiosurgery alone in patients with newly diagnosed brain metastases (Results and implications) . Int J Radiat Oncol Biol Phys . 2002;52:333–338
  83. Monje ML , Mizumatsu S , Fike JR , et al.   Irradiation induces neural precursor-cell dysfunction . Nat Med . 2002;8:955–962
  84. Senzer N . Rationale for a phase III study of erythropoietin as a neurocognitive protectant in patients with lung cancer receiving prophylactic cranial irradiation . Semin Oncol . 2002;29:47–52
  85. Sakanaka M , Wen TC , Matsuda S , et al.   In vivo evidence that erythropoietin protects neurons from ischemic damage . Proc Natl Acad Sci USA . 1998;95:4635–4640
  86. Masuda S , Okano M , Yamagishi K , et al.   A novel site of erythropoietin production. Oxygen-dependent production in cultured rat astrocytes . J Biol Chem . 1994;269:19488–19493
  87. Bernaudin M , Bellail A , Marti HH , et al.   Neurons and astrocytes express EPO mRNA (Oxygen-sensing mechanisms that involve the redox-state of the brain) . Glia . 2000;30:271–278
  88. Morishita E , Masuda S , Nagao M , et al.   Erythropoietin receptor is expressed in rat hippocampal and cerebral cortical neurons, and erythropoietin prevents in vitro glutamate-induced neuronal death . Neuroscience . 1997;76:105–116
  89. Hengemihle JM , Abugo O , Rifkind J , et al.   Chronic treatment with human recombinant erythropoietin increases hematocrit and improves water maze performance in mice . Physiol Behav . 1996;59:153–156
  90. Catania MA , Marciano MC , Parisi A , et al.   Erythropoietin prevents cognition impairment induced by transient brain ischemia in gerbils . Eur J Pharmacol . 2002;437:147–150
  91. Fike JR , Gobbel GT , Marton LJ , et al.   Radiation brain injury is reduced by the polyamine inhibitor alpha-difluoromethylornithine . Radiat Res . 1994;138:99–106
  92. Kondziolka D , Mori Y , Martinez AJ , et al.   Beneficial effects of the radioprotectant 21-aminosteroid U-74389G in a radiosurgery rat malignant glioma model . Int J Radiat Oncol Biol Phys . 1999;44:179–184
  93. Weitzner MA , Meyers CA , Valentine AD . Methylphenidate in the treatment of neurobehavioral slowing associated with cancer and cancer treatment . J Neuropsychiatry Clin Neurosci . 1995;7:347–350
  94. DeLong R , Friedman H , Friedman N , et al.   Methylphenidate in neuropsychological sequelae of radiotherapy and chemotherapy of childhood brain tumors and leukemia . J Child Neurol . 1992;7:462–463
  95. Meyers CA , Weitzner MA , Valentine AD , et al.   Methylphenidate therapy improves cognition, mood, and function of brain tumor patients . J Clin Oncol . 1998;16:2522–2527
  96. Plafki C , Carl UM , Glag M , et al.   The treatment of late radiation effects with hyperbaric oxygenation (HBO) . Strahlenther Onkol . 1998;174(suppl 3):66–68
  97. Hulshof MC , Stark NM , van der Kleij A , et al.   Hyperbaric oxygen therapy for cognitive disorders after irradiation of the brain . Strahlenther Onkol . 2002;178:192–198
  98. Groves AK , Barnett SC , Franklin RJ , et al.   Repair of demyelinated lesions by transplantation of purified O-2A progenitor cells . Nature . 1993;362:453–455
  99. Brustle O , Jones KN , Learish RD , et al.   Embryonic stem cell-derived glial precursors (A source of myelinating transplants) . Science . 1999;285:754–756
  100. Brugmann M , Schlager A , Schubert A , et al.   Neuropsychological effects of preventive CNS irradiation in adult tumor patients . Psychother Psychosom Med Psychol . 1998;48:375–380
  101. Ahles TA , Silberfarb PM , Herndon J , et al.   Psychologic and neuropsychologic functioning of patients with limited small-cell lung cancer treated with chemotherapy and radiation therapy with or without warfarin (A study by the Cancer and Leukemia Group B) . J Clin Oncol . 1998;16:1954–1960
  102. Crossen JR , Garwood D , Glatstein E , et al.   Neurobehavioral sequelae of cranial irradiation in adults (A review of radiation-induced encephalopathy) . J Clin Oncol . 1994;12:627–642
  103. Cull A , Gregor A , Hopwood P , et al.   Neurological and cognitive impairment in long-term survivors of small cell lung cancer . Eur J Cancer . 1994;8:1067–1074
  104. Lishner M , Feld R , Payne DG , et al.   Late neurological complications after prophylactic cranial irradiation in patients with small-cell lung cancer (The Toronto experience) . J Clin Oncol . 1990;8:215–221
  105. Laukkanen E , Klonoff H , Allan B , et al.   The role of prophylactic brain irradiation in limited stage small cell lung cancer (Clinical, neuropsychologic, and CT sequelae) . Int J Radiat Oncol Biol Phys . 1988;14:1109–1117
  106. Chak LY , Zatz LM , Wasserstein P , et al.   Neurologic dysfunction in patients treated for small cell carcinoma of the lung (A clinical and radiological study) . Int J Radiat Oncol Biol Phys . 1986;12:385–389
  107. Catane R , Schwade JG , Yarr I , et al.   Follow-up neurological evaluation in patients with small cell lung carcinoma treated with prophylactic cranial irradiation and chemotherapy . Int J Radiat Oncol Biol Phys . 1981;7:105–109
  108. Glosser G , McManus P , Munzenrider J , et al.   Neuropsychological function in adults after high dose fractionated radiation therapy of skull base tumors . Int J Radiat Oncol Biol Phys . 1997;38:231–239
  109. Kleinberg L , Wallner K , Malkin MG . Good performance status of long-term disease-free survivors of intracranial gliomas . Int J Radiat Oncol Biol Phys . 1993;26:129–133
  110. Ferreri AJ , Reni M , Dell’Oro S , et al.   Combined treatment with high-dose methotrexate, vincristine and procarbazine, without intrathecal chemotherapy, followed by consolidation radiotherapy for primary central nervous system lymphoma in immunocompetent patients . Oncology . 2001;60:134–140
  111. Abrey LE , Yahalom J , DeAngelis LM . Treatment for primary CNS lymphoma (The next step) . J Clin Oncol . 2000;18:3144–3150
  112. O’Neill BP , Wang CH , O’Fallon JR , et al.   The consequences of treatment and disease in patients with primary CNS non-Hodgkin’s lymphoma (Cognitive function and performance status) . North Central Cancer Treatment Group. Neurooncology . 1999;1:196–203
  113. Boiardi A , Silvani A , Pozzi A , et al.   Chemotherapy is effective as early treatment for primary central nervous system lymphoma . J Neurol . 1999;246:31–37
  114. Shibamoto Y , Sasai K , Oya N , et al.   Systemic chemotherapy with vincristine, cyclophosphamide, doxorubicin and prednisolone following radiotherapy for primary central nervous system lymphoma (A phase II study) . J Neurooncol . 1999;42:161–167
  115. Abrey LE , DeAngelis LM , Yahalom J . Long-term survival in primary CNS lymphoma . J Clin Oncol . 1998;16:859–863
  116. Glass J , Gruber ML , Cher L , et al.   Preirradiation methotrexate chemotherapy of primary central nervous system lymphoma (Long-term outcome) . J Neurosurg . 1994;81:188–195

PII: S0093-7754(04)00335-5

doi: 10.1053/j.seminoncol.2004.07.013

Seminars in Oncology
Volume 31, Issue 5 , Pages 702-713 , October 2004