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01-05-2015 | Topic Review

Review of cranial radiotherapy-induced vasculopathy

Authors: Erin S. Murphy, Hao Xie, Thomas E. Merchant, Jennifer S. Yu, Samuel T. Chao, John H. Suh

Published in: Journal of Neuro-Oncology | Issue 3/2015

Abstract

Cranial radiation can impact the cerebral vasculature in many ways, with a wide range of clinical manifestations. The incidence of these late effects including cerebrovascular accidents (CVAs), lacunar lesions, vascular occlusive disease including moyamoya syndrome, vascular malformations, and hemorrhage is not well known. This article reviews the preclinical findings regarding the pathophysiology of late radiation-induced vascular damage, and discusses the clinical incidence and risk factors for each type of vasculopathy. The pathophysiology is complex and dependent on the targeted blood vessels, and upregulation of pro-inflammatory and hypoxia-related genes. The risk factors for adult CVAs are similar to those for patients not exposed to cranial radiotherapy. For children, risks for late vascular complications include young age at radiotherapy, radiotherapy dose, NF1, tumor location, chemotherapy, and endocrine abnormalities. The incidence of late vascular complications of radiotherapy may be impacted by improved technology, therapeutic interventions, and appropriate follow up.

Kortmann R-D, Timmermann B, Taylor RE, Scarzello G, Plasswilm L, Paulsen F, Jeremic B, Gnekow AK, Dieckmann K, Kay S (2003) Current and future strategies in radiotherapy of childhood low-grade glioma of the brain. Strahlenther Onkol 179:509–520

Hall EJ, Giaccia AJ (2006) Clinical response of normal tissues. Radiobiol Radiol 6:333–337

Ljubimova NV, Levitman MK, Plotnikova ED, Eidus LK (1991) Endothelial cell population dynamics in rat brain after local irradiation. Br J Radiol 64:934–940CrossRefPubMed

Li Y-Q, Chen P, Jain V, Reilly RM, Wong CS (2004) Early radiation-induced endothelial cell loss and blood–spinal cord barrier breakdown in the rat spinal cord. Radiat Res 161:143–152CrossRefPubMed

Li Y-Q, Chen P, Haimovitz-Friedman A, Reilly RM, Wong CS (2003) Endothelial apoptosis initiates acute blood–brain barrier disruption after ionizing radiation. Cancer Res 63:5950–5956PubMed

Reinhold HS, Calvo W, Hopewell JW, den Berg AP (1990) Development of blood vessel-related radiation damage in the fimbria of the central nervous system. Int J Radiat Oncol* Biol* Phys 18:37–42CrossRef

van der Kogel AJ (1986) Radiation-induced damage in the central nervous system: an interpretation of target cell responses. Br J Cancer Suppl 7:207–217PubMedCentralPubMed

Gabrail NY, Harrison BR, Sunwoo YC (1991) Chemo-irradiation induced aortoesophageal fistula. J Surg Oncol 48:213–215CrossRefPubMed

McCready RA, Hyde GL, Bivins BA, Mattingly SS, Griffen WO Jr (1983) Radiation-induced arterial injuries. Surgery (US) 93:306–312

10.

Stewart FA, Heeneman S, te Poele J, Kruse J, Russell NS, Gijbels M, Daemen M (2006) Ionizing radiation accelerates the development of atherosclerotic lesions in ApoE<sup>−/− mice and predisposes to an inflammatory plaque phenotype prone to hemorrhage. Am J Pathol 168:649–658CrossRefPubMedCentralPubMed

11.

Price RA, Birdwell DA (1978) The central nervous system in childhood leukemia. III. Mineralizing microangiopathy and dystrophic calcification. Cancer 42:717–728CrossRefPubMed

12.

Hong J-H, Chiang C-S, Campbell IL, Sun J-R, Withers HR, McBride WH (1995) Induction of acute phase gene expression by brain irradiation. Int J Radiat Oncol* Biol* Phys 33:619–626CrossRef

13.

Soares MP, Seldon MP, Gregoire IP, Vassilevskaia T, Berberat PO, Yu J, Tsui T-Y, Bach FH (2004) Heme oxygenase-1 modulates the expression of adhesion molecules associated with endothelial cell activation. J Immunol 172:3553–3563CrossRefPubMed

14.

Kim JH, Brown SL, Jenrow KA, Ryu S (2008) Mechanisms of radiation-induced brain toxicity and implications for future clinical trials. J Neurooncol 87:279–286CrossRefPubMed

15.

Li Y-Q, Ballinger JR, Nordal RA, Su Z-F, Wong CS (2001) Hypoxia in radiation-induced blood–spinal cord barrier breakdown. Cancer Res 61:3348–3354PubMed

16.

Brada M, Ashley S, Ford D, Traish D, Burchell L, Rajan B (2002) Cerebrovascular mortality in patients with pituitary adenoma. Clin Endocrinol (Oxf) 57:713–717CrossRef

17.

Brada M, Burchell L, Ashley S, Traish D (1999) The incidence of cerebrovascular accidents in patients with pituitary adenoma. Int J Radiat Oncol Biol Phys 45:693–698CrossRefPubMed

18.

Erfurth EM, Bulow B, Svahn-Tapper G, Norrving B, Odh K, Mikoczy Z, Bjork J, Hagmar L (2002) Risk factors for cerebrovascular deaths in patients operated and irradiated for pituitary tumors. J Clin Endocrinol Metab 87:4892–4899CrossRefPubMed

19.

Flickinger JC, Nelson PB, Taylor FH, Robinson A (1989) Incidence of cerebral infarction after radiotherapy for pituitary adenoma. Cancer 63:2404–2408CrossRefPubMed

20.

Sattler MG, Vroomen PC, Sluiter WJ, Schers HJ, van den Berg G, Langendijk JA, Wolffenbuttel BH, van den Bergh AC, van Beek AP (2013) Incidence, causative mechanisms, and anatomic localization of stroke in pituitary adenoma patients treated with postoperative radiation therapy versus surgery alone. Int J Radiat Oncol Biol Phys 87:53–59CrossRefPubMed

21.

Bowers DC, Mulne AF, Reisch JS, Elterman RD, Munoz L, Booth T, Shapiro K, Doxey DL (2002) Nonperioperative strokes in children with central nervous system tumors. Cancer 94:1094–1101CrossRefPubMed

22.

Bowers DC, Liu Y, Leisenring W, McNeil E, Stovall M, Gurney JG, Robison LL, Packer RJ, Oeffinger KC (2006) Late-occurring stroke among long-term survivors of childhood leukemia and brain tumors: a report from the Childhood Cancer Survivor Study. J Clin Oncol 24:5277–5282CrossRefPubMed

23.

Omura M, Aida N, Sekido K, Kakehi M, Matsubara S (1997) Large intracranial vessel occlusive vasculopathy after radiation therapy in children: clinical features and usefulness of magnetic resonance imaging. Int J Radiat Oncol* Biol* Phys 38:241–249CrossRef

24.

Campen CJ, Kranick SM, Kasner SE, Kessler SK, Zimmerman RA, Lustig R, Phillips PC, Storm PB, Smith SE, Ichord R, Fisher MJ (2012) Cranial irradiation increases risk of stroke in pediatric brain tumor survivors. Stroke 43:3035–3040

25.

Grill J, Couanet D, Cappelli C, Habrand JL, Rodriguez D, Sainte-Rose C, Kalifa C (1999) Radiation-induced cerebral vasculopathy in children with neurofibromatosis and optic pathway glioma. Ann Neurol 45:393–396CrossRefPubMed

26.

Crom DB, Smith D, Xiong Z, Onar A, Hudson MM, Merchant TE, Morris EB (2010) Health status in long-term survivors of pediatric craniopharyngiomas. J Neurosci Nurs 42:323–328; quiz 329–330

27.

Liu AK, Bagrosky B, Fenton LZ, Gaspar LE, Handler MH, McNatt SA, Foreman NK (2009) Vascular abnormalities in pediatric craniopharyngioma patients treated with radiation therapy. Pediatr Blood Cancer 52:227–230CrossRefPubMed

28.

Fouladi M, Langston J, Mulhern R, Jones D, Xiong X, Yang J, Thompson S, Walter A, Heideman R, Kun L, Gajjar A (2000) Silent lacunar lesions detected by magnetic resonance imaging of children with brain tumors: a late sequela of therapy. J Clin Oncol 18:824

29.

Cheng K-M, Chan C-M, Fu Y-T, Ho L-C, Cheung F-C, Law C-K (2001) Acute hemorrhage in late radiation necrosis of the temporal lobe: report of five cases and review of the literature. J Neurooncol 51:143–150CrossRefPubMed

30.

Poussaint TY, Siffert J, Barnes PD, Pomeroy SL, Goumnerova LC, Anthony DC, Sallan SE, Tarbell NJ (1995) Hemorrhagic vasculopathy after treatment of central nervous system neoplasia in childhood: diagnosis and follow-up. Am J Neuroradiol 16:693–699PubMed

31.

Lew SM, Morgan JN, Psaty E, Lefton DR, Allen JC, Abbott R (2006) Cumulative incidence of radiation-induced cavernomas in long-term survivors of medulloblastoma. J Neurosurg Pediatr 104:103–107CrossRef

32.

Strenger V, Sovinz P, Lackner H, Dornbusch HJ, Lingitz H, Eder HG, Moser A, Urban C (2008) Intracerebral cavernous hemangioma after cranial irradiation in childhood. Incidence and risk factors. Strahlenther Onkol 184:276–280CrossRefPubMed

33.

Nimjee SM, Powers CJ, Bulsara KR (2006) Review of the literature on de novo formation of cavernous malformations of the central nervous system after radiation therapy. Neurosurg Focus 21:1–6CrossRef

34.

Epsfein MA, Packer RJ, Rorke LB, Zimmerman RA, Goldwein JW, Sutton LN, Schut L (1992) Vascular malformation with radiation vasculopathy after treatment of chiasmatic/hypothalamic glioma. Cancer 70:887–893CrossRef

35.

Heckl S, Aschoff A, Kunze S (2002) Radiation-induced cavernous hemangiomas of the brain. Cancer 94:3285–3291CrossRefPubMed

36.

Burn S, Gunny R, Phipps K, Gaze M, Hayward R (2007) Incidence of cavernoma development in children after radiotherapy for brain tumors. J Neurosurg Pediatr 106:379–383CrossRef

37.

Koike S, Aida N, Hata M, Fujita K, Ozawa Y, Inoue T (2004) Asymptomatic radiation-induced telangiectasia in children after cranial irradiation: frequency, latency, and dose relation1. Radiology 230:93–99CrossRefPubMed

38.

Sciubba DM, Gallia GL, Recinos P, Garonzik IM, Clatterbuck RE (2006) Intracranial aneurysm following radiation therapy during childhood for a brain tumor: case report and review of the literature. J Neurosurg Pediatr 105:134–139CrossRef

39.

Kikuchi A, Maeda M, Hanada R, Okimoto Y, Ishimoto K, Kaneko T, Ikuta K, Tsuchida M (2007) Moyamoya syndrome following childhood acute lymphoblastic leukemia. Pediatr Blood Cancer 48:268–272CrossRefPubMed

40.

Desai SS, Paulino AC, Mai WY, Teh BS (2006) Radiation-induced moyamoya syndrome. Int J Radiat Oncol* Biol* Phys 65:1222–1227CrossRef

41.

Kestle JRW, Hoffman HJ, Mock AR (1993) Moyamoya phenomenon after radiation for optic glioma. J Neurosurg 79:32–35CrossRefPubMed

42.

Ullrich NJ, Robertson R, Kinnamon DD, Scott RM, Kieran MW, Turner CD, Chi SN, Goumnerova L, Proctor M, Tarbell NJ, Marcus KJ, Pomeroy SL (2007) Moyamoya following cranial irradiation for primary brain tumors in children. Neurology 68:932–938

43.

Rudoltz MS, Regine WF, Langston JW, Sanford RA, Kovnar EH, Kun LE (1998) Multiple causes of cerebrovascular events in children with tumors of the parasellar region. J Neurooncol 37:251–261CrossRefPubMed

44.

Pollock BE, Nippoldt TB, Stafford SL, Foote RL, Abboud CF (2002) Results of stereotactic radiosurgery in patients with hormone-producing pituitary adenomas: factors associated with endocrine normalization. J Neurosurg 97:525–530CrossRefPubMed

45.

Lim YJ, Leem W, Park JT, Kim TS, Rhee BA, Kim GK (1999) Cerebral infarction with ICA occlusion after Gamma Knife radiosurgery for pituitary adenoma: a case report. Stereotact Funct Neurosurg 72(Suppl 1):132–139CrossRefPubMed

46.

Gross BA, Ropper AE, Du R (2013) Vascular complications of stereotactic radiosurgery for arteriovenous malformations. Clin Neurol Neurosurg 115:713–717CrossRefPubMed

47.

Quigg M, Yen CP, Chatman M, Quigg AH, McNeill IT, Przybylowski CJ, Yan G, Sheehan JP (2012) Risks of history of diabetes mellitus, hypertension, and other factors related to radiation-induced changes following Gamma Knife surgery for cerebral arteriovenous malformations. J Neurosurg 117(Suppl):144–149PubMed

48.

Harrod-Kim P, Kadkhodayan Y, Derdeyn CP, Cross DT III, Moran CJ (2005) Outcomes of carotid angioplasty and stenting for radiation-associated stenosis. Am J Neuroradiol 26:1781–1788PubMed

49.

Mohr JP, Parides MK, Stapf C, Moquete E, Moy CS, Overbey JR, Al-Shahi Salman R, Vicaut E, Young WL, Houdart E, Cordonnier C, Stefani MA, Hartmann A, von Kummer R, Biondi A, Berkefeld J, Klijn CJ, Harkness K, Libman R, Barreau X, Moskowitz AJ (2014) Medical management with or without interventional therapy for unruptured brain arteriovenous malformations (ARUBA): a multicentre, non-blinded, randomised trial. Lancet 383:614–621CrossRefPubMedCentralPubMed

50.

Yu SC, Zou WX, Soo YO, Wang L, Hui JW, Chan AY, Lee KT, Ip VH, Fan FS, Chan AL, Wong LK, Leung TW (2014) Evaluation of carotid angioplasty and stenting for radiation-induced carotid stenosis. Stroke 45:1402–1407CrossRefPubMed

51.

Bowers DC (2009) Strokes among brain tumor survivors. In: Goldman S, Turner CD (eds) Late effects of treatment for brain tumors. Springer, New York, NY, pp 145–153

52.

Shih HA, Loeffler JS, Tarbell NJ (2009) Late Effects of CNS Radiation Therapy. In: Goldman S, Turner CD (eds) Late effects of treatment for brain tumors. Springer, New York, NY, pp 23–41

53.

Monje ML, Toda H, Palmer TD (2003) Inflammatory blockade restores adult hippocampal neurogenesis. Science 302:1760–1765CrossRefPubMed

54.

Sadraei NH, Dahiya S, Chao ST, Murphy ES, Osei-Boateng K, Xie H, Suh JH, Peereboom DM, Stevens GH, Ahluwalia MS (2013) Treatment of cerebral radiation necrosis with bevacizumab: The Cleveland Clinic experience. Am J Clin Oncol. 10.1097/COC.0b013e31829c3139

55.

Morris B, Partap S, Yeom K, Gibbs IC, Fisher PG, King AA (2009) Cerebrovascular disease in childhood cancer survivors A Children’s Oncology Group Report. Neurology 73:1906–1913CrossRefPubMedCentralPubMed

56.

Laitt RD, Chambers EJ, Goddard PR, Wakeley CJ, Duncan AW, Foreman NK (1995) Magnetic resonance imaging and magnetic resonance angiography in long term survivors of acute lymphoblastic leukemia treated with cranial irradiation. Cancer 76:1846–1852CrossRefPubMed

Title: Review of cranial radiotherapy-induced vasculopathy
Authors: Erin S. Murphy
Hao Xie
Thomas E. Merchant
Jennifer S. Yu
Samuel T. Chao
John H. Suh
Publication date: 01-05-2015
Publisher: Springer US
Published in: Journal of Neuro-Oncology / Issue 3/2015
Print ISSN: 0167-594X
Electronic ISSN: 1573-7373
DOI: https://doi.org/10.1007/s11060-015-1732-2

At a glance: The STEP trials

Springer Medicine

Review of cranial radiotherapy-induced vasculopathy

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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