Vascular endothelial growth factor inhibitors and cognitive impairment: Evidence and controversies

Expert Opinion on Drug Safety

Volumn 13, Issue 1, 2014, Pages 83-92

  Ng, Terence ^a   Cheung, Yin Ting ^a   Ng, Quan Sing ^b   Ho, Han Kiat ^a   Chan, Alexandre ^a  

^a NATIONAL UNIVERSITY OF SINGAPORE   (Singapore)

^b DIVISION OF MEDICAL ONCOLOGY   (Singapore)

Author keywords

Bevacizumab; Cognition; Pazopanib; Sorafenib; Sunitinib; Vascular endothelial growth factor

Indexed keywords

BEVACIZUMAB; PAZOPANIB; SORAFENIB; SUNITINIB; UNCLASSIFIED DRUG; VASCULOTROPIN; VASCULOTROPIN INHIBITOR; VATALANIB; ZK 222574;

CANCER CHEMOTHERAPY; CANCER PATIENT; COGNITION; COGNITIVE DEFECT; DISEASE ASSOCIATION; DRUG TARGETING; HUMAN; MALIGNANT NEOPLASTIC DISEASE; NEUROTOXICITY; NONHUMAN; REVIEW;

ANGIOGENESIS INHIBITORS; ANIMALS; ANTINEOPLASTIC AGENTS; COGNITION; COGNITION DISORDERS; HUMANS; NEOPLASMS; NEOVASCULARIZATION, PATHOLOGIC; SEVERITY OF ILLNESS INDEX; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84890452226     PISSN: 14740338     EISSN: 1744764X     Source Type: Journal    
DOI: 10.1517/14740338.2013.828034     Document Type: Review

References (102)

1. Schagen SB, Vardy J. Cognitive dysfunction in people with cancer. Lancet Oncol 2007;8:852-3 (Pubitemid 47488056)
2. Vardy J. Cognitive function in breast cancer survivors. Cancer Treat Res 2009;151:387-419
3. Hurria A, Somlo G, Ahles T. Renaming chemobrain. Cancer Invest 2007;25:373-7
4. Cheung YT, Shwe M, Tan YP, et al. Cognitive changes in multiethnic Asian breast cancer patients: a focus group study. Ann Oncol 2012;10:2547-52
5. Cheung YT, Shwe M, Chui WK, et al. Effects of chemotherapy and psychosocial distress on perceived cognitive disturbances in asian breast cancer patients. Ann Pharmacother 2012;46:1645-55
6. Cheung YT, Chui WK, Chan A. Neuro-cognitive impairment in breast cancer patients: pharmacological considerations. Crit Rev Oncol Hematol 2012;83:99-111
7. Pullens MJ, De Vries J, Roukema JA. Subjective cognitive dysfunction in breast cancer patients: a systematic review. Psychooncology 2010;19:1127-38
8. Reid-Arndt SA, Hsieh C, Perry MC. Neuropsychological functioning and quality of life during the first year after completing chemotherapy for breast cancer. Psychooncology 2010;19:535-44
9. Ferrara N, Gerber HP, LeCouter J. The biology of VEGF and its receptors. Nat Med 2003;9:669-76 (Pubitemid 36749215)
10. Mackenzie F, Ruhrberg C. Diverse roles for VEGF-A in the nervous system. Development 2012;139:1371-80
11. Ruiz de Almodovar C, Lambrechts D, Mazzone M, et al. Role and therapeutic potential of VEGF in the nervous system. Physiol Rev 2009;89:607-48
12. Shojaei F. Anti-Angiogenesis therapy in cancer: current challenges and future perspectives. Cancer Lett 2012;320:130-7
13. Cook KM, Figg WD. Angiogenesis inhibitors: current strategies and future prospects. CA Cancer J Clin 2010;60:222-43
14. Palmer TD, Willhoite AR, Gage FH. Vascular niche for adult hippocampal neurogenesis. J Comp Neurol 2000;425:479-94
15. Shen Q, Goderie SK, Jin L, et al. Endothelial cells stimulate self-renewal and expand neurogenesis of neural stem cells. Science 2004;304:1338-40 (Pubitemid 38697433)
16. Bao X, Wei J, Feng M, et al. Transplantation of human bone marrow-derived mesenchymal stem cells promotes behavioral recovery and endogenous neurogenesis after cerebral ischemia in rats. Brain Res 2011;1367:103-13
17. Cao L, Jiao X, Zuzga DS, et al. VEGF links hippocampal activity with neurogenesis, learning and memory. Nat Genet 2004;36:827-35 (Pubitemid 39014099)
18. Wong-Goodrich SJ, Pfau ML, Flores CT, et al. Voluntary running prevents progressive memory decline and increases adult hippocampal neurogenesis and growth factor expression after whole-brain irradiation. Cancer Res 2010;70:9329-38
19. Olsson AK, Dimberg A, Kreuger J, et al. VEGF receptor signalling - in control of vascular function. Nat Rev Mol Cell Biol 2006;7:359-71
20. Banks WA. Characteristics of compounds that cross the blood-brain barrier. BMC Neurol 2009;9:S3
21. Fabel K, Fabel K, Tam B, et al. VEGF is necessary for exercise-induced adult hippocampal neurogenesis. Eur J Neurosci 2003;18:2803-12 (Pubitemid 37542133)
22. Kim BW, Choi M, Kim YS, et al. Vascular endothelial growth factor (VEGF) signaling regulates hippocampal neurons by elevation of intracellular calcium and activation of calcium/calmodulin protein kinase II and mammalian target of rapamycin. Cell Signal 2008;20:714-25
23. Licht T, Goshen I, Avital A, et al. Reversible modulations of neuronal plasticity by VEGF. Proc Natl Acad Sci USA 2011;108:5081-6
24. Sun Y, Jin K, Childs JT, et al. Vascular endothelial growth factor-B (VEGFB) stimulates neurogenesis: evidence from knockout mice and growth factor administration. Dev Biol 2006;289:329-35 (Pubitemid 43049936)
25. Calvo CF, Fontaine RH, Soueid J, et al. Vascular endothelial growth factor receptor 3 directly regulates murine neurogenesis. Genes Dev 2011;25:831-44
26. Dobrogowska DH, Lossinsky AS, Tarnawski M, et al. Increased blood-brain barrier permeability and endothelial abnormalities induced by vascular endothelial growth factor. J Neurocytol 1998;27:163-73 (Pubitemid 28253067)
27. Byrne AM, Bouchier-Hayes DJ, Harmey JH. Angiogenic and cell survival functions of vascular endothelial growth factor (VEGF). J Cell Mol Med 2005;9:777-94 (Pubitemid 43116546)
28. Ruitenberg A, den Heijer T, Bakker SL, et al. Cerebral hypoperfusion and clinical onset of dementia: The Rotterdam Study. Ann Neurol 2005;57:789-94 (Pubitemid 40798616)
29. Poels MM, Ikram MA, Vernooij MW, et al. Total cerebral blood flow in relation to cognitive function: The Rotterdam Scan Study. J Cereb Blood Flow Metab 2008;28:1652-5
30. Austin BP, Nair VA, Meier TB, et al. Effects of hypoperfusion in Alzheimers disease. J Alzheimers Dis 2011;26 Suppl 3:123-33
31. Kalaria RN, Cohen DL, Premkumar DR, et al. Vascular endothelial growth factor in Alzheimers disease and experimental cerebral ischemia. Brain Res Mol Brain Res 1998;62:101-5 (Pubitemid 29023185)
32. Hai J, Li ST, Lin Q, et al. Vascular endothelial growth factor expression and angiogenesis induced by chronic cerebral hypoperfusion in rat brain. Neurosurgery 2003;53:963-70; discussion 70-2
33. Wang P, Xie ZH, Guo YJ, et al. VEGF-induced angiogenesis ameliorates the memory impairment in APP transgenic mouse model of Alzheimers disease. Biochem Biophys Res Commun 2011;411:620-6
34. Yang SP, Bae DG, Kang HJ, et al. Co-Accumulation of vascular endothelial growth factor with beta-Amyloid in the brain of patients with Alzheimers disease. Neurobiol Aging 2004;25:283-90 (Pubitemid 38220962)
35. Deng W, Aimone JB, Gage FH. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat Rev Neurosci 2010;11:339-50
36. Couillard-Despres S, Iglseder B, Aigner L. Neurogenesis, cellular plasticity and cognition: The impact of stem cells in the adult and aging brain-A mini-review. Gerontology 2011;57:559-64
37. Izquierdo I, Medina JH. Memory formation: The sequence of biochemical events in the hippocampus and its connection to activity in other brain structures. Neurobiol Learn Mem 1997;68:285-316 (Pubitemid 27506324)
38. Eichenbaum H. A cortical-hippocampal system for declarative memory. Nat Rev Neurosci 2000;1:41-50
39. Eichenbaum H. The hippocampus and declarative memory: cognitive mechanisms and neural codes. Behav Brain Res 2001;127:199-207 (Pubitemid 33062410)
40. Morris RG. Elements of a neurobiological theory of hippocampal function: The role of synaptic plasticity, synaptic tagging and schemas. Eur J Neurosci 2006;23:2829-46 (Pubitemid 43882862)
41. Koehl M, Abrous DN. A new chapter in the field of memory: adult hippocampal neurogenesis. Eur J Neurosci 2011;33:1101-14
42. Sahay A, Hen R. Adult hippocampal neurogenesis in depression. Nat Neurosci 2007;10:1110-15 (Pubitemid 47339960)
43. Sahay A, Scobie KN, Hill AS, et al. Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 2011;472:466-70
44. Plaschke K, Staub J, Ernst E, et al. VEGF overexpression improves mice cognitive abilities after unilateral common carotid artery occlusion. Exp Neurol 2008;214:285-92
45. Michalczyk K, Ziman M. Nestin structure and predicted function in cellular cytoskeletal organisation. Histol Histopathol 2005;20:665-71 (Pubitemid 40468283)
46. Benjamin LE, Hemo I, Keshet E. A plasticity window for blood vessel remodelling is defined by pericyte coverage of the preformed endothelial network and is regulated by PDGF-B and VEGF. Development 1998;125:1591-8 (Pubitemid 28256727)
47. Cameron HA, Hazel TG, McKay RD. Regulation of neurogenesis by growth factors and neurotransmitters. J Neurobiol 1998;36:287-306 (Pubitemid 28363237)
48. Lee E, Son H. Adult hippocampal neurogenesis and related neurotrophic factors. BMB Rep 2009;42:239-44
49. Bliss TV, Collingridge GL. A synaptic model of memory: long-Term potentiation in the hippocampus. Nature 1993;361:31-9 (Pubitemid 23020772)
50. Cooke SF, Bliss TV. Plasticity in the human central nervous system. Brain 2006;129:1659-73 (Pubitemid 43999401)
51. Pati S, Orsi SA, Moore AN, et al. Intra-hippocampal administration of the VEGF receptor blocker PTK787/ZK222584 impairs long-Term memory. Brain Res 2009;1256:85-91
52. van der Veldt AA, van den Eertwegh AJ, Hoekman K, et al. Reversible cognitive disorders after sunitinib for advanced renal cell cancer in patients with preexisting arteriosclerotic leukoencephalopathy. Ann Oncol 2007;18:1747-50 (Pubitemid 47506267)
53. Schuff N, Matsumoto S, Kmiecik J, et al. Cerebral blood flow in ischemic vascular dementia and Alzheimers disease, measured by arterial spin-labeling magnetic resonance imaging. Alzheimers Dement 2009;5:454-62
54. Mulder SF, Bertens D, Vissers KCP, et al. Impairment of cognitive functioning during sunitinib or sorafenibtreatment-A cross sectional study. Eur J Cancer 2011;47:S514; Po7132
55. Noal S, Lange M, Escudier B, et al. Fatigue, quality of life, and cognitive functions in metastatic kidney cancer patients with antiangiogenic treatment. Ann Oncol 2010;21:S8, viii298; abstract 950
56. AVASTIN (bevacizumab). Genentech, Inc; South San Francisco, CA: 2012
57. Friedman HS, Prados MD, Wen PY, et al. Bevacizumab alone and in combination with irinotecan in recurrent glioblastoma. J Clin Oncol 2009;27:4733-40
58. Kreisl TN, Kim L, Moore K, et al. Phase II trial of single-Agent bevacizumab followed by bevacizumab plus irinotecan at tumor progression in recurrent glioblastoma. J Clin Oncol 2009;27:740-5
59. Tang SC, Lagas JS, Lankheet NA, et al. Brain accumulation of sunitinib is restricted by P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) and can be enhanced by oral elacridar and sunitinib coadministration. Int J Cancer 2012;130:223-33
60. Tang SC, Lankheet NA, Poller B, et al. P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) restrict brain accumulation of the active sunitinib metabolite N-desethyl sunitinib. J Pharmacol Exp Ther 2012;341:164-73
61. Boykoff N, Moieni M, Subramanian SK. Confronting chemobrain: an in-depth look at survivors reports of impact on work, social networks, and health care response. J Cancer Surviv 2009;3:223-32
62. Debess J, Riis JO, Engebjerg MC, et al. Cognitive function after adjuvant treatment for early breast cancer: a population-based longitudinal study. Breast Cancer Res Treat 2010;121:91-100
63. Bender CM, Sereika SM, Berga SL, et al. Cognitive impairment associated with adjuvant therapy in breast cancer. Psychooncology 2006;15:422-30 (Pubitemid 43826855)
64. Ahles TA, Saykin AJ, McDonald BC, et al. Longitudinal assessment of cognitive changes associated with adjuvant treatment for breast cancer: impact of age and cognitive reserve. J Clin Oncol 2010;28:4434-40
65. Hermelink K, Untch M, Lux MP, et al. Cognitive function during neoadjuvant chemotherapy for breast cancer: results of a prospective, multicenter, longitudinal study. Cancer 2007;109:1905-13 (Pubitemid 46668557)
66. Jansen CE, Cooper BA, Dodd MJ, et al. A prospective longitudinal study of chemotherapy-induced cognitive changes in breast cancer patients. Support Care Cancer 2011;19:1647-56
67. Jansen CE, Dodd MJ, Miaskowski CA, et al. Preliminary results of a longitudinal study of changes in cognitive function in breast cancer patients undergoing chemotherapy with doxorubicin and cyclophosphamide. Psychooncology 2008;17:1189-95
68. Jenkins V, Shilling V, Deutsch G, et al. A 3-year prospective study of the effects of adjuvant treatments on cognition in women with early stage breast cancer. Br J Cancer 2006;94:828-34
69. Jim HS, Donovan KA, Small BJ, et al. Cognitive functioning in breast cancer survivors: a controlled comparison. Cancer 2009;115:1776-83
70. Mehlsen M, Pedersen AD, Jensen AB, et al. No indications of cognitive side-effects in a prospective study of breast cancer patients receiving adjuvant chemotherapy. Psychooncology 2009;18:248-57
71. Quesnel C, Savard J, Ivers H. Cognitive impairments associated with breast cancer treatments: results from a longitudinal study. Breast Cancer Res Treat 2009;116:113-23
72. Schagen SB, Muller MJ, Boogerd W, et al. Change in cognitive function after chemotherapy: a prospective longitudinal study in breast cancer patients. J Natl Cancer Inst 2006;98:1742-5 (Pubitemid 44942713)
73. Stewart A, Collins B, Mackenzie J, et al. The cognitive effects of adjuvant chemotherapy in early stage breast cancer: a prospective study. Psychooncology 2008;17:122-30 (Pubitemid 351279862)
74. Tchen N, Juffs HG, Downie FP, et al. Cognitive function, fatigue, and menopausal symptoms in women receiving adjuvant chemotherapy for breast cancer. J Clin Oncol 2003;21:4175-83 (Pubitemid 46606186)
75. Tager FA, McKinley PS, Schnabel FR, et al. The cognitive effects of chemotherapy in post-menopausal breast cancer patients: a controlled longitudinal study. Breast Cancer Res Treat 2010;123:25-34
76. van Dam FS, Schagen SB, Muller MJ, et al. Impairment of cognitive function in women receiving adjuvant treatment for high-risk breast cancer: high-dose versus standard-dose chemotherapy. J Natl Cancer Inst 1998;90:210-18 (Pubitemid 28114539)
77. Wefel JS, Lenzi R, Theriault RL, et al. The cognitive sequelae of standard-dose adjuvant chemotherapy in women with breast carcinoma: results of a prospective, randomized, longitudinal trial. Cancer 2004;100:2292-9 (Pubitemid 38657875)
78. Wefel JS, Vardy J, Ahles T, et al. International Cognition and Cancer Task Force recommendations to harmonise studies of cognitive function in patients with cancer. Lancet Oncol 2011;12:703-8
79. Holmes D. Trying to unravel the mysteries of chemobrain. Lancet Neurol 2013;12(6):533-4
80. Asher A. Cognitive dysfunction among cancer survivors. Am J Phys Med Rehabil 2011;90:S16-26
81. Ahles TA, Saykin AJ, McDonald BC, et al. Longitudinal assessment of cognitive changes associated with adjuvant treatment for breast cancer: impact of age and cognitive reserve. J Clin Oncol 2010;28:4434-40
82. OConnor JP, Jackson A, Asselin MC, et al. Quantitative imaging biomarkers in the clinical development of targeted therapeutics: current and future perspectives. Lancet Oncol 2008;9:766-76 (Pubitemid 352038315)
83. Peterson B, Summergrad P. Binswangers disease (Part II): pathogenesis of subcortical arteriosclerotic encephalopathy and its relation to other dementing processes. J Geriatr Psychiatry Neurol 1989;2:171-81 (Pubitemid 20142159)
84. Leritz EC, McGlinchey RE, Kellison I, et al. Cardiovascular disease risk factors and cognition in the elderly. Curr Cardiovasc Risk Rep 2011;5:407-12
85. Del Bo R, Ghezzi S, Scarpini E, et al. VEGF genetic variability is associated with increased risk of developing Alzheimers disease. J Neurol Sci 2009;283:66-8
86. Del Bo R, Scarlato M, Ghezzi S, et al. Vascular endothelial growth factor gene variability is associated with increased risk for AD. Ann Neurol 2005;57:373-80 (Pubitemid 40343959)
87. Chiappelli M, Borroni B, Archetti S, et al. VEGF gene and phenotype relation with Alzheimers disease and mild cognitive impairment. Rejuvenation Res 2006;9:485-93 (Pubitemid 46100670)
88. Chapuis J, Tian J, Shi J, et al. Association study of the vascular endothelial growth factor gene with the risk of developing Alzheimers disease. Neurobiol Aging 2006;27:1212-15 (Pubitemid 44067310)
89. Mateo I, Llorca J, Infante J, et al. Case-control study of vascular endothelial growth factor (VEGF) genetic variability in Alzheimers disease. Neurosci Lett 2006;401:171-3 (Pubitemid 44269286)
90. SUTENT (sunitinib malate). Pfizer Inc., New York, NY: 2012
91. Patyna S, Peng J. Distribution of sunitinib and its active metabolite in brain and spinal cord tissue following oral or intravenous administration in rodents and monkeys [abstract 56]. Eur J Cancer 2006;4:21
92. Thibault F, Billemont B, Rixe O. Regression of brain metastases of renal cell carcinoma with antiangiogenic therapy. J Neurooncol 2008;86:243-4 (Pubitemid 350263426)
93. Zeng H, Li X, Yao J, et al. Multifocal brain metastases in clear cell renal cell carcinoma with complete response to sunitinib. Urol Int 2009;83:482-5
94. Koutras AK, Krikelis D, Alexandrou N, et al. Brain metastasis in renal cell cancer responding to sunitinib. Anticancer Res 2007;27:4255-7
95. Medioni J, Cojocarasu O, Belcaceres JL, et al. Complete cerebral response with sunitinib for metastatic renal cell carcinoma. Ann Oncol 2007;18:1282-3 (Pubitemid 47244377)
96. NEXAVAR (sorafenib). Bayer Pharmaceuticals Corp; West Haven, CT: 2011
97. Kim A, McCully C, Cruz R, et al. The plasma and cerebrospinal fluid pharmacokinetics of sorafenib after intravenous administration in non-human primates. Invest New Drugs 2012;30:524-8
98. Agarwal MM, Khandelwal N, Mandal AK, et al. Factors affecting bone mineral density in patients with prostate carcinoma before and after orchidectomy. Cancer 2005;103:2042-52 (Pubitemid 40605111)
99. Agarwal S, Elmquist WF. Insight into the cooperation of P-glycoprotein (ABCB1) and breast cancer resistance protein (ABCG2) at the blood-brain barrier: a case study examining sorafenib efflux clearance. Mol Pharm 2012;9:678-84
100. Minocha M, Khurana V, Qin B, et al. Enhanced brain accumulation of pazopanib by modulating P-gp and Bcrp1 mediated efflux with canertinib or erlotinib. Int J Pharm 2012;436:127-34
101. VOTRIENT (pazopanib). GlaxoSmithKline; Research Triangle Park, NC: 2012
102. Iwamoto FM, Lamborn KR, Robins HI, et al. Phase II trial of pazopanib (GW786034), an oral multi-Targeted angiogenesis inhibitor, for adults with recurrent glioblastoma (North American Brain Tumor Consortium Study 06-02). Neuro Oncol 2010;12:855-61