Disruption of learning processes by chemotherapeutic agents in child-hood survivors of acute lymphoblastic leukemia and preclinical models

Journal of Cancer

Volumn 2, Issue 1, 2011, Pages 292-301

  Bisen Hersh, Emily B ^a   Hineline, Philip N ^a   Walker, Ellen A ^a,b  

^a TEMPLE UNIVERSITY   (United States)

^b TEMPLE UNIVERSITY SCHOOL OF PHARMACY   (United States)

Author keywords

Acute lymphoblastic leukemia; Chemotherapy; Childhood cancer; Cognitive late effects; Preclinical models

Indexed keywords

ANTINEOPLASTIC AGENT; ASPARAGINASE; CARMUSTINE; CISPLATIN; CORTICOSTEROID; CYCLOPHOSPHAMIDE; CYTARABINE; DEXAMETHASONE; DOXORUBICIN; FLUOROURACIL; HYDROCORTISONE; MERCAPTOPURINE; METHOTREXATE; METHYLPHENIDATE; PREDNISOLONE; PREDNISONE; VINCRISTINE;

ACUTE LYMPHOBLASTIC LEUKEMIA; BLOOD BRAIN BARRIER; BRAIN DAMAGE; BRAIN DEVELOPMENT; CANCER SURVIVOR; CHILDHOOD CANCER; COGNITIVE DEFECT; CYTOTOXICITY; HUMAN; LEARNING; LEUKOENCEPHALOPATHY; MEDICAL EDUCATION; MEDICAL LITERATURE; NEUROPHYSIOLOGY; NEUROTOXICITY; NONHUMAN; REVIEW; SURVIVAL RATE; TASK PERFORMANCE; WORKING MEMORY;

EID: 84878966706     PISSN: None     EISSN: 18379664     Source Type: Journal    
DOI: 10.7150/jca.2.292     Document Type: Review

References (89)

1. [Internet] Children's Oncology Group. Establishing and en-hancing services for childhood cancer survivors: long-term follow-up program resource guide. http://www.survivorshipguidelines.org/.
2. Moleski M. Neuropsychological, neuroanatomical, and neuro-physiological consequences of CNS chemotherapy for acutelymphoblastic leukemia. Arch Clin Neuropsych. 2000; 15: 603-630.
3. Oeffinger KC, Mertens AC, Sklar CA, et al. Chronic health conditions in adult survivors of childhood cancer. N Engl J Med. 2006; 355: 1572-1582.
4. Krull KR, Okcu MF, Potter B, et al. Screening for neurocognitive impairment in pediatric cancer long-term survivors. J Clin Oncol. 2008; 26: 4138-4143.
5. Bowers DC, Liu Y, Leisenring W, et al. Late-occurring stroke among long-term survivors of childhood leukemia and brain tumors: a report from the childhood cancer survivor study. J Clin Oncol. 2006; 24: 5277-5282.
6. Mulrooney DA, Dover DC, Li S, et al. Twenty years of follow-up among survivors of childhood and young adult acute myeloid leukemia. Cancer. 2008; 112: 2071-2079.
7. Kadan-Lottick NS, Zeltzer LK, Liu Q, et al. Neurocognitive functioning in adult survivors of childhood non-central nervous system cancers. JNCI. 2010; 102: 881-893.
8. Leisenring WM, Mertens AC, Armstrong GT, et al. Pediatric cancer survivorship research: experience of the childhood cancer survivor study. J Clin Oncol. 2009; 27: 2319-2327.
9. Pui C & Evans WE. Treatment of acute lymphoblastic leukemia. N Engl J Med. 2006; 354: 166-178.
10. Buizer AI, de Sonneville LMJ, & Veerman AJP. Effects of chemotherapy on neurocognitive function in children with acute lymphoblastic leukemia: a critical review of the literature. Pediatr Blood and Cancer. 2009; 52: 447-454.
11. Janzen LA, & Spiegler BJ. Neurodevelopmental sequelae of pediatric acute lymphoblastic leukemia and its treatment. Dev Dis Rev. 2008; 14: 185-95.
12. Butler RW & Haser JK. Neurocognitive effects of treatment for childhood cancer. Ment Retard Dev Dis Rev. 2006; 12: 184-191.
13. Mulhern RK & Butler RW. Neurocognitive sequelae of child-hood cancers and their treatment. Pediatr Rehabilitation. 2004; 7: 1-14.
14. Stehbens JA, Kaleita TA, Noll RB, et al. CNS prophylaxis of childhood leukemia: what are the long-term neurological, neuropsychological, and behavioral effects? Neuropsychol Rev. 1991; 2: 147-177.
15. Pui C, Campana D, Pei D, et al. Treatment of childhood acute lymphoblastic leukemia without prophylactic cranial irradiation. N Engl J Med. 2009; 360: 2730-2741.
16. Leung W, Hudson M, Zhu Y, et al. Late effects of survivors of infant leukemia. Leukemia. 2000; 14: 1185-1190.
17. Haupt R, Fears TR, Robinson LL, et al. Educational attainment in long-term survivors of childhood acute lymphoblastic leukemia. JAMA. 1994; 272: 1427-1432.
18. Kingma A, Rammeloo LAJ, van der Does-van den Berg A, et al. Academic career after treatment for acute lymphoblastic leu-kaemia. Arch Dis Child. 2000; 82: 353-357.
19. Brown RT, Madan-Swain A, Pais R, et al. Chemotherapy for acute lymphocytic leukemia: cognitive and academic sequelae. J Pediatr. 1992; 121: 885-889.
20. Taylor, HG, Albo VC, Phebus C, et al. Post irradiation treatment outcomes for children with acute lymphocytic leukemia. J Pediatr Psychol. 1987; 12: 394-411.
21. Moss HA, Nannis ED, & Poplack DG. The effects of prophylactic treatment of the central nervous system on the intellectual functioning of children with acute lymphocytic leukemia. Am J Med. 1981; 71: 47-52.
22. Jankovic M, Brouwers P, Valsecchi MG, et al. Association of 1800 cGy cranial irradiation with intellectual function in chil-dren with acute lymphoblastic leukaemia. Lancet. 1994; 344: 224-227.
23. Mulhern RK, Fairclough D, & Ochs J. A prospective comparison of neuropsychologic performance of children surviving leuke-mia who received 18-Gy, 24-Gy, or no cranial irradiation. J Clin Oncol. 1991; 9: 1348-1356.
24. Giralt J, Ortega JJ, Olive T, et al. Long-term neuropsychologic sequelae of childhood leukemia: comparison of two CNS prophylactic regimens. Int J Radiat Oncol. 1992; 24: 49-53.
25. Espy KA, Moore IM, Kaufmann PM, et al. Chemotherapeutic CNS prophylaxis and neuropsychologic change in children with acute lymphoblastic leukemia: a prospective study. J Pediatr Psychol. 2001; 26: 1-9.
26. Seigers R, Timmermans J, van der Horn HJ, et al. Methotrexate reduces hippocampal blood vessel density and activates mi-croglia in rats but does not elevate central cytokine release. Behav Brain Res. 2010; 207: 265-272.
27. Krull KR, Brouwers P, Neelam J, et al. Pathway genetic polymorphisms are related to attention disorders in childhood leukemia survivors. J Pediatr. 2008; 152: 101-105.
28. Rodgers J, Horrocks J, Britton PG, et al. Attentional ability among survivors of leukaemia. Arch Dis Child. 1999; 80: 318-323.
29. Langer T, Martus P, Ottensmeier H, et al. CNS late-effects after ALL therapy in childhood. Part III: Neuropsychological performance in long-term survivors of childhood ALL: impairments of concentration, attention, and memory. Med Pediatr Oncol. 2002; 38: 320-328.
30. Schatz J, Kramer JH, Ablin AR, et al. Visual attention in long-term survivors of leukemia receiving cranial radiation therapy. J Int Neuropsychol Soc. 2004; 10: 211-220.
31. Lockwood KA, Bell TS, & Colegrove RW. Long-term effects of cranial radiation therapy on attentional functioning in survi-vors of childhood leukemia. J Pediatr Psychol. 1999; 24: 55-66.
32. Buizer AI, de Sonneville LMJ, van den Heuvel-Eibrink MM, et al. Chemotherapy and attentional dysfunction in survivors of childhood acute lymphoblastic leukemia. Pediatr Blood Cancer. 2005; 45: 281-290.
33. Schatz J, Kramer JH, Ablin A, et al. Processing speed, working memory, and IQ: a developmental model of cognitive deficits following cranial radiation therapy. Neuropsychology. 2000; 14: 189-200.
34. Ashford J, Schoffstall C, Reddick WE, et al. Attention and working memory abilities in children treated for acute lym-phoblastic leukemia. Cancer. 2010; 116: 4638-4645.
35. Mennes M, Stiers P, Vandenbussche E, et al. Attention and information processing in survivors of childhood acute lym-phoblastic leukemia treated with chemotherapy only. Pediatr Blood Cancer. 2005; 44: 479-486.
36. Campbell LK, Scaduto M, Sharp W, et al. A meta-analysis of the neurocognitve sequelae of treatment for childhood acute lym-phocytic leukemia. Pediatr Blood Cancer. 2007; 49: 65-73.
37. Jain N, Brouwers P, Okcu M, et al. Sex-specific attention problems in long-term survivors of pediatric acute lymphoblastic leukemia. Cancer. 2009; 115: 4238-4245.
38. Spiegler BJ, Kennedy K, Maze R, et al. Comparison of long-term neurocognitive outcomes in young children with acute lym-phoblastic leukemia treated with cranial radiation or high-dose or very high-dose intravenous methotrexate. J Clin Oncol. 2006; 24: 3858-3864.
39. Waber DP, Turek J, Catania L, et al. Neuropsychological out-comes from a randomized trial of triple intrathecal chemo-therapy compared with 18 gy cranial radiation as CNS treatment in acute lymphoblastic leukemia: findings from Da-na-Farber cancer institute ALL consortium protocol 95-01. J Clin Oncol. 2007; 25: 4914-4921.
40. Kadan-Lottick NS, Brouwers P, Breiger D, et al. Comparison of neurocognitive functioning in children previously randomly assigned to intrathecal therapy for the treatment of childhood acute lymphoblastic leukemia. J Clin Oncol. 2009; 27: 5986-5992.
41. Vardy J, Wefel JS, Ahles T, et al. Cancer and cancer-therapy related cognitive dysfunction: an international perspective from the venice cognitive workshop. Ann Oncol. 2008; 19: 623-629.
42. Reddick WE, & Conklin HM. Impact of acute lymphoblastic leukemia therapy on attention and working memory in children. Expert Rev Hematol. 2010; 3: 655-659.
43. Waber DP, Carpentieri SC, Klar N, et al. Cognitive sequelae in children treated for acute lymphoblastic leukemia with dexa-methasone or prednisone. J Pediatr Hematol Oncol. 2000; 22: 206-213.
44. Ochs, JJ. Neurotoxicity due to central nervous system therapy for childhood leukemia. Am J Pediatr Hematol Oncol. 1989; 11: 93-105.
45. Lee YY, Nauert C, & Glass P. Treatment-related white matter changes in cancer patients. Cancer. 1986; 57: 1473-1482.
46. Reddick WE, White HA, Glass JO, et al. Developmental model relating white matter volume to neurocognitive deficits in pe-diatric brain tumor survivors. Cancer. 2003; 97: 2512-2519.
47. Steinberg S, Hartmann R, Wisniewski S, et al. Late sequelae of CNS recurrence of acute lymphoblastic leukemia in childhood. Klin Padiatr. 1998; 210: 200-206.
48. Filley CM. The behavioral neurology of cerebral white matter. Neurology. 1998; 50: 1535-1540.
49. Ciesielski KT, Lesnik PG, Sanders JA, et al. MRI morphometry of mamillary bodies, caudate nuclei, and prefrontal cortices after chemotherapy for childhood leukemia: multivariate models of early and late developing memory subsystems. Behav Neurosci. 1999; 113: 439-450.
50. Dietrich J, Han R, Yang Y, et al. CNS progenitor cells and oligodendrocytes are targets of chemotherapeutic agents in vitro and in vivo. J Biol. 2006; 5: 22.1-22.
51. Janelsins MC, Roscoe JA, Berg MJ, et al. IGF-1 partially restores chemotherapy-induced reductions in neural cell proliferation in adult C57BL/6 mice. Cancer Invest. 2010; 28: 544-553.
52. Ahles TA & Saykin AJ. Candidate mechanisms for chemotherapy-induced cognitive changes. Nat Rev Cancer. 2007; 7: 192-201.
53. Seigers R & Fardell JE. Neurobiological basis of chemotherapy-induced cognitive impairment: a review of rodent research. Neurosci Biobehav Rev. 2011; 35: 729-741.
54. Rubenstein CL, Varni JW, & Katz ER. Cognitive functioning in long-term survivors of childhood leukemia: a prospective analysis. J Dev Behav Pediatr. 1990; 11: 301-305.
55. Raffa RB, Duong PV, Finney J, et al. Is 'chemo-fog'/'chemo-brain' caused by cancer chemotherapy? J Clin Pharm Ther. 2006; 31: 129-138.
56. Stock HS, Rosellini RA, Abrahamsen GC, et al. Methotrexate does not interfere with an appetitive pavlovian conditioning task in sprague-dawley rats. Physiol Behav. 1995; 58: 969-973.
57. Yadin E, Bruno L, Micalizzi M, et al. An animal model to detect learning deficits following treatment of the immature brain. Child's Brain. 1983; 10: 273-280.
58. Yanovski JA, Packer RJ, Levine JD, et al. An animal model to detect the neuropsychological toxicity of anticancer agents. Med Pediatr Oncol. 1989; 17: 216-221.
59. Conklin HM, Helton S, Ashford J, et al. Predicting methylphenidate response in long-term survivors of childhood cancer: a randomized, double-blind, placebo-controlled, cross-over trial. J Pediatr Psychol. 2010; 35: 144-155.
60. Conklin HM, Khan RB, Reddick WE, et al. Acute neurocognitive response to methylphenidate among survivors of child-hood cancer: a randomized, double-blind, cross-over trial. J Pediatr Psychol. 2007; 32: 1127-1139.
61. Waber DP, Tarbell NJ, Fairclough D, et al. Cognitive sequelae of treatment in childhood acute lymphoblastic leukemia: cranial radiation requires an accomplice. J Clin Oncol. 1995; 13: 2490-2496.
62. Waber DP, Tarbell NJ, Kahn CM, et al. The relationship of sex and treatment modality to neuropsychologic outcome in childhood acute lymphoblastic leukemia. J Clin Oncol. 1992; 10: 810-817.
63. Seigers R, Schagen SB, Beerling W, et al. Long-lasting suppression of hippocampal cell proliferation and impaired cognitive performance by methotrexate in the rat. Behav Brain Res. 2008; 186: 168-175.
64. Madhyastha S, Somayaji SN, Rao MS, et al. Hippocampal brain amines in methotrexate-induced learning and memory deficit. Can J Physiol Pharmacol. 2002; 80: 1076-1084.
65. Igarashi H, Inomata K, & Tateno A. The effect of methotrexate on the development of synapses in the neonatal rat hippo-campus. Neuropediatrics. 1989; 20: 196-198.
66. Silverstein FS & Johnston MV. A model of methotrexate en-cephalopathy: neurotransmitter and pathologic abnormalities. J Child Neurol. 1986; 1: 351-357.
67. Foley JJ, Raffa RB, & Walker EA. Effects of chemotherapeutic agents 5-fluorouracil and methotrexate alone and combined in a mouse model of learning and memory. Psychopharmacology. 2008; 199: 527-538.
68. Winocur G, Vardy J, Binns MA, et al. The effects of anti-cancer drugs, methotrexate and 5-fluorouracil on cognitive function in mice. Pharmacol Biochem Behav. 2006; 85: 66-75.
69. Walker EA. Animal Models. In: Raffa RB and Tallarida RJ, ed. 'Chemo-fog': Cancer Chemotherapy-Related Cognitive Im-pairment. US: Landes Bioscience. 2010.
70. Chen D, Fu Wu C, Shi B, et al. Tamoxifen and toremifene cause impairment of learning and memory function in mice. Pharmacol Biochem Behav. 2002; 71: 269-276.
71. El-Beltagy M, Mustafa S, Umka J, et al. Fluoxetine improves the memory deficits caused by the chemotherapy agent 5-fluorouracil. Behav Brain Res. 2010; 208: 112-117.
72. Lyons L, ElBeltagy M, Umka J, et al. Fluoxetine reverses the memory impairment and reduction in proliferation and sur-vival of hippocampal cells caused by methotrexate chemotherapy. Psychopharmacology. 2011; 215: 105-115.
73. van Praag H, Mei Qu P, Elliott RC, et al. Unilateral hippocampal lesions in newborn and adult rats: effects on spatial memory and BDNF gene expression. Behav Brain Res. 1998; 92: 21-30.
74. Mullenix PJ, Kernan WJ, Schunior A, et al. Interactions of steroid, methotrexate, and radiation determine neurotoxicity in an animal model to study therapy for childhood leukemia. Pediatr Res. 1994; 35: 171-178.
75. Sapolsky RM. A mechanism for glucocorticoid toxicity in the hippocampus: increased neuronal vulnerability to metabolic insults. J Neurosci. 1985; 5: 1228-1232.
76. Li CQ, Liu D, Huang L, et al. Cytosine arabinoside treatment impairs the remote spatial memory function and induces den-dritic retraction in the anterior cingulate cortex of rats. Brain Res Bull. 2008; 77: 237-240.
77. Borzan J, LaGraize SC, & Fuchs PN. Effect of chronic vincristine treatment on mechanical withdrawal response and pre-pulse inhibition in the rat. Neurosci Lett. 2004; 364: 110-113.
78. Eijkenboom M & Van Der Staay FJ. Spatial learning deficits in rats after injection of vincristine into the dorsal hippocampus. Neuroscience. 1999; 91: 1299-1313.
79. Liedke PE, Reolon GK, Kilpp B, et al. Systemic administration of doxorubicin impairs aversively motivated memory in rats. Pharmacol Biochem Behav. 2009; 94: 239-243.
80. Sieklucka-Dziuba M, Saczonek J, Dziuba J, et al. Central action of some cytostatics-methotrexate (MTX) and doxorubicin (DXR): II. The influence on the seizure activity and the learning and memory processes in mice. Ann Univ Mariae Curie Sklodowska. 1998; 53: 81-88.
81. Macleod JE, DeLeo JA, Hickey WF, et al. Cancer chemotherapy impairs contextual but not cue-specific fear memory. Behav Brain Res. 2007; 181: 168-172.
82. Konat GW, Kraszpulski M, James I, et al. Cognitive dysfunction induced by chronic administration of common cancer chemo-therapeutics in rats. Metab Brain Dis. 2008; 23: 325-333.
83. Heyser CJ. Assessment of developmental milestones in rodents. Curr Protoc Neurosci. 2003; 25: 8.18.1-8.18.15.
84. Laviola G, Macri S, Morley-Fletcher S, et al. Risk-taking behavior in adolescent mice: psychobiological determinants and early epigenetic influence. Neurosci Biobehav Rev. 2003; 27: 19-31.
85. Boyette-Davis JA & Fuchs PN. Differential effects of paclitaxel treatment on cognitive functioning and mechanical sensitivity. Neurosci Lett. 2009; 453: 170-174.
86. Mondie CM, Vandergrift KA, Wilson CL, et al. The chemo-therapy agent, thioTEPA, yields long-term impairment of hip-pocampal cell proliferation and memory deficits but not de-pression-related behaviors in mice. Behav Brain Res. 2010; 209: 66-72.
87. Arnold HM, Bruno JP, & Sarter M. Assessment of sustained and divided attention in rats. Curr Protoc Neurosci. 2003; 22: 8.5E.1-8.5E.13.
88. Seigers R, Pourtau L, Schagen SB, et al. Inhibition of hippo-campal cell proliferation by methotrexate in rats is not potenti-ated by the presence of a tumor. Brain Res Bull. 2010; 81: 472-476.
89. Krull KR, Gioia G, Ness KK, et al. Reliability and validity of the childhood cancer survivor study neurocognitive questionnaire. Cancer. 2008; 113: 2188-97.