Hostname: page-component-78c5997874-lj6df Total loading time: 0 Render date: 2024-11-10T07:21:02.709Z Has data issue: false hasContentIssue false
  • English
  • Français

Visuomotor control in survivors of childhood acute lymphoblastic leukemia treated with chemotherapy only

Published online by Cambridge University Press:  26 August 2005

ANNEMIEKE I. BUIZER ,
LEO M.J. DE SONNEVILLE ,
MARRY M. VAN DEN HEUVEL-EIBRINK ,
CHARLES NJIOKIKTJIEN  and
ANJO J.P. VEERMAN
ANNEMIEKE I. BUIZER
Affiliation:
Department of Pediatrics, VU University Medical Center, Amsterdam, The Netherlands
LEO M.J. DE SONNEVILLE
Affiliation:
Department of Pediatrics, VU University Medical Center, Amsterdam, The Netherlands
MARRY M. VAN DEN HEUVEL-EIBRINK
Affiliation:
Department of Pediatric Hemato-Oncology, Erasmus Medical Center/Sophia Children's Hospital, Rotterdam, The Netherlands
CHARLES NJIOKIKTJIEN
Affiliation:
Department of Pediatrics, VU University Medical Center, Amsterdam, The Netherlands
ANJO J.P. VEERMAN
Affiliation:
Department of Pediatrics, VU University Medical Center, Amsterdam, The Netherlands
Get access Rights & Permissions [Opens in a new window]

Abstract

Treatment for childhood acute lymphoblastic leukemia (ALL), which includes CNS prophylaxis, is associated with central and peripheral neurotoxicity. The purpose of the present study was to analyze the effects of chemotherapy on various levels of visuomotor control in survivors of childhood ALL treated without cranial irradiation, and to identify risk factors for possible deficits. Visuomotor function was compared between children after treatment for ALL (n = 34), children after treatment for Wilms tumor, which consists of non-CNS directed chemotherapy (n = 38), and healthy controls (n = 151). Three tasks were administered: a simple visual reaction time task and two tasks measuring visuomotor control with one requiring a higher level of cognitive control than the other. Visuomotor deficits were detected only in the ALL group, with poorer performance restricted to the condition requiring the highest level of control. Significant risk factors for poorer performance were female gender and a short time since end of treatment, and a trend was found for a young age at diagnosis. A high cumulative methotrexate dose was an adverse predictive factor in girls. The results indicate that chemotherapy-induced central neurotoxicity in childhood ALL treatment is associated with higher order visuomotor control deficits. Girls appear to be particularly vulnerable. (JINS, 2005, 11, 554–565.)

Keywords

Psychomotor performanceNeoplasmsDrug therapyAdverse effectsChildAdolescent
Type
Research Article
Information
Journal of the International Neuropsychological Society , Volume 11 , Issue 5 , September 2005 , pp. 554 - 565
Copyright
© 2005 The International Neuropsychological Society

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

REFERENCES

Aiken, L.S. & West, S.G. (1991). Multiple regression: Testing and interpreting interactions. Newbury Park, CA: Sage Publications.
Anderson, V.A., Godber, T., Smibert, E., Weiskop, S., & Ekert, H. (2000). Cognitive and academic outcome following cranial irradiation and chemotherapy in children: A longitudinal study. British Journal of Cancer, 82, 255–262.Google Scholar
Brown, R.T., Madan-Swain, A., Pais, R., Lambert, R.G., Baldwin, K., Casey, R., Frank, N., Sexson, S.B., Ragab, A., & Kamphaus, R.W. (1992). Cognitive status of children treated with central nervous system prophylactic chemotherapy for acute lymphocytic leukemia. Archives of Clinical Neuropsychology, 7, 481–497.Google Scholar
Brown, R.T., Madan-Swain, A., Walco, G.A., Cherrick, I., Ievers, C.E., Conte, P.M., Vega, R., Bell, B., & Lauer, S.J. (1998). Cognitive and academic late effects among children previously treated for acute lymphocytic leukemia receiving chemotherapy as CNS prophylaxis. Journal of Pediatric Psychology, 23, 333–340.Google Scholar
Butler, R.W., Hill, J.M., Steinherz, P.G., Meyers, P.A., & Finlay, J.L. (1994). Neuropsychologic effects of cranial irradiation, intrathecal methotrexate, and systemic methotrexate in childhood cancer. Journal of Clinical Oncology, 12, 2621–2629.Google Scholar
Carbone, P.P., Bono, V., Frei, E., III, & Brindley, C.O. (1963). Clinical studies with vincristine. Blood, 21, 640–647.Google Scholar
Chaminade, T. & Fonlupt, P. (2003). Changes of effective connectivity between the lateral and medial parts of the prefrontal cortex during a visual task. European Journal of Neuroscience, 18, 675–679.Google Scholar
Chu, W.C., Chik, K.W., Chan, Y.L., Yeung, D.K., Roebuck, D.J., Howard, R.G., Li, C.K., & Metreweli, C. (2003). White matter and cerebral metabolite changes in children undergoing treatment for acute lymphoblastic leukemia: Longitudinal study with MR imaging and 1H MR spectroscopy. Radiology, 229, 659–669.Google Scholar
Ciesielksi, K.T., Harris, R.J., Hart, B.L., & Pabst, H.F. (1997). Cerebellar hypoplasia and frontal lobe cognitive deficits in disorders of early childhood. Neuropsychologia, 35, 643–655.Google Scholar
Ciesielski, K.T., Lesnik, P.G., Benzel, E.C., Hart, B.L., & Sanders, J.A. (1999). MRI morphometry of mamillary bodies, caudate nuclei, and prefrontal cortices after chemotherapy for childhood leukemia: Multivariate models of early and late developing memory subsystems. Behavioral Neuroscience, 113, 439–450.Google Scholar
Cohen, J. (1988). Statistical power analysis for the behavioral sciences (2nd ed.). Hillsdale, NJ: Lawrence Earlbaum Associates.
Copeland, D.R., Moore, B.D., Francis, D.J., Jaffe, N., & Culbert, S.J. (1996). Neuropsychologic effects of chemotherapy on children with cancer: A longitudinal study. Journal of Clinical Oncology, 14, 2826–2835.Google Scholar
Cousens, P., Waters, B., Said, J., & Stevens, M. (1988). Cognitive effects of cranial irradiation in leukaemia: A survey and meta-analysis. Journal of Child Psychology and Psychiatry, 29, 839–852.Google Scholar
D'Angio, G.J. (1983). SIOP (International Society of Paediatric Oncology) and the management of Wilms' tumor. Journal of Clinical Oncology, 1, 595–596.Google Scholar
Dambska, M. & Laure-Kamionowska, M. (1999). Brain damage in children in course of neoplastic diseases. Folia Neuropathologica, 37, 133–137.Google Scholar
De Bellis, M.D., Keshavan, M.S., Beers, S.R., Hall, J., Frustaci, K., Masalehdan, A., Noll, J., & Boring, A.M. (2001). Sex differences in brain maturation during childhood and adolescence. Cerebral Cortex, 11, 552–557.Google Scholar
De Sonneville, L.M.J. (1999). Amsterdam Neuropsychological Tasks: A computer-aided assessment program. In B.P.L.M. den Brinker, P.J. Beek, A.N. Brand, S.J. Maarse, & L.J.M. Mulder (Eds.), Cognitive ergonomics, clinical assessment and computer-assisted learning: Computers in psychology (pp. 187–203). Lisse, The Netherlands: Swets & Zeitlinger.
De Sonneville, L.M.J. (2003). Amsterdam Neuropsychological Tasks, Manual: Database and Appendix. Amstelveen, The Netherlands: SONAR.
De Sonneville, L.M.J., Boringa, J.B., Reuling, I.E.W., Lazeron, R.H.C., Adèr, H.J., & Polman, C.H. (2002). Information processing characteristics in subtypes of multiple sclerosis. Neuropsychologia, 40, 1751–1765.Google Scholar
DeAngelis, L.M., Gnecco, C., Taylor, L., & Warrell, R.P., Jr. (1991). Evolution of neuropathy and myopathy during intensive vincristine/corticosteroid chemotherapy for non-Hodgkin's lymphoma. Cancer, 67, 2241–2246.Google Scholar
Diamond, A. (2000). Close interrelation of motor development and cognitive development and of the cerebellum and prefrontal cortex. Child Development, 71, 44–56.Google Scholar
Downie, A.L.S., Jakobson, L.S., Frisk, V., & Ushycky, I. (2003). Periventricular brain injury, visual motion processing, and reading and spelling abilities in children who were extremely low birthweight. Journal of the International Neuropsychological Society, 9, 440–449.Google Scholar
Erickson, K., Baron, I.S., & Fantie, B.D. (2001). Neuropsychological functioning in early hydrocephalus: Review from a developmental perspective. Child Neuropsychology, 7, 199–229.Google Scholar
Frank, E.G., Foley, G.M., & Kuchuk, A. (1997). Cognitive functioning in school-age children with human immunodeficiency virus. Perceptual and Motor Skills, 85, 267–272.Google Scholar
Fuster, J.M. (2002). Frontal lobe and cognitive development. Journal of Neurocytology, 31, 373–385.Google Scholar
Galea, V., Wright, M.J., & Barr, R.D. (2004). Measurement of balance in survivors of acute lymphoblastic leukemia in childhood. Gait & Posture, 19, 1–10.Google Scholar
Gatta, G., Capocaccia, R., Coleman, M.P., Ries, L.A., & Berrino, F. (2002). Childhood cancer survival in Europe and the United States. Cancer, 95, 1767–1772.Google Scholar
Gidding, C.E., Kellie, S.J., Kamps, W.A., & de Graaf, S.S. (1999). Vincristine revisited. Critical Reviews in Oncology/Hematology, 29, 267–287.Google Scholar
Glickstein, M. (2000). How are visual areas of the brain connected to motor areas for the sensory guidance of movement? Trends in Neuroscience, 23, 613–617.Google Scholar
Hamzei, F., Dettmers, C., Rijntjes, M., Glauche, V., Kiebel, S., Weber, B., & Weiller, C. (2002). Visuomotor control within a distributed parieto-frontal network. Experimental Brain Research, 146, 273–281.Google Scholar
Harila-Saari, A.H., Huuskonen, U.E.J., Tolonen, U., Vainionpaa, L.K., & Lanning, B.M. (2001). Motor nervous pathway function is impaired after treatment of childhood acute lymphoblastic leukemia: A study with motor evoked potentials. Medical and Pediatric Oncology, 36, 345–351.Google Scholar
Harila-Saari, A.H., Vainionpaa, L.K., Kovala, T.T., Tolonen, E.U., & Lanning, B.M. (1998). Nerve lesions after therapy for childhood acute lymphoblastic leukemia. Cancer, 82, 200–207.Google Scholar
Heitger, M.H., Anderson, T.J., Jones, R.D., Dalrymple-Alford, J.C., Frampton, C.M., & Ardagh, M.W. (2004). Eye movement and visuomotor arm movement deficits following mild closed head injury. Brain, 127, 575–590.Google Scholar
Huijbregts, S.C., De Sonneville, L.M., Van Spronsen, F.J., Berends, I.E., Licht, R., Verkerk, P.H., & Sergeant, J.A. (2003). Motor function under lower and higher controlled processing demands in early and continuously treated phenylketonuria. Neuropsychology, 17, 369–379.Google Scholar
Jakobson, L.S., Frisk, V., Knight, R.M., Downie, A.L.S., & Whyte, H. (2001). The relationship between periventricular brain injury and deficits in visual processing among extremely-low-birthweight (< 1000 g) children. Journal of Pediatric Psychology, 26, 503–512.Google Scholar
Jankovic, M., Brouwers, P., Valsecchi, M.G., Van Veldhuizen, A., Huisman, J., Kamphuis, R., Kingma, A., Mor, W., Van Dongen-Melman, J., & Ferronato, L. (1994). Association of 1800 cGy cranial irradiation with intellectual function in children with acute lymphoblastic leukaemia. ISPACC. International Study Group on Psychosocial Aspects of Childhood Cancer. Lancet, 344, 224–227.Google Scholar
Kalff, A.C., de Sonneville, L.M., Hurks, P.P., Hendriksen, J.G., Kroes, M., Feron, F.J., Steyaert, J., van Zeben, T.M., Vles, J.S., & Jolles, J. (2003). Low- and high-level controlled processing in executive motor control tasks in 5–6-year-old children at risk of ADHD. Journal of Child Psychology and Psychiatry, 44, 1049–1057.Google Scholar
Kamps, W.A., Bokkerink, J.P., Hahlen, K., Hermans, J., Riehm, H., Gadner, H., Schrappe, M., Slater, R., van den Berg-de Ruiter, E., Smets, L.A., De Vaan, G.A., Weening, R.S., van Weerden, J.F., Van Wering, E.R., & van der Does-van den Berg, A. (1999). Intensive treatment of children with acute lymphoblastic leukemia according to ALL-BFM-86 without cranial radiotherapy: Results of Dutch Childhood Leukemia Study Group Protocol ALL-7 (1988–1991). Blood, 94, 1226–1236.Google Scholar
Kamps, W.A., Bokkerink, J.P., Hakvoort-Cammel, F.G., Veerman, A.J., Weening, R.S., Van Wering, E.R., van Weerden, J.F., Hermans, J., Slater, R., van den Berg, E., Kroes, W.G., & van der Does-van den Berg, A. (2002). BFM-oriented treatment for children with acute lymphoblastic leukemia without cranial irradiation and treatment reduction for standard risk patients: Results of DCLSG protocol ALL-8 (1991–1996). Leukemia, 16, 1099–1111.Google Scholar
Kellie, S.J., Barbaric, D., Koopmans, P., Earl, J., Carr, D.J., & de Graaf, S.S.N. (2002). Cerebrospinal fluid concentrations of vincristine after bolus intravenous dosing—A surrogate marker of brain penetration. Cancer, 94, 1815–1820.Google Scholar
Kerr, J.Z., Berg, S., & Blaney, S.M. (2001). Intrathecal Chemotherapy. Critical Reviews in Oncology/Hematology, 37, 227–236.Google Scholar
Kingma, A., Van Dommelen, R.I., Mooyaart, E.L., Wilmink, J.T., Deelman, B.G., & Kamps, W.A. (2001). Slight cognitive impairment and magnetic resonance imaging abnormalities but normal school levels in children treated for acute lymphoblastic leukemia with chemotherapy only. Journal of Pediatrics, 139, 413–420.Google Scholar
Klingberg, T., Vaidya, C.J., Gabrieli, J.D.E., Moseley, M.E., & Hedehus, M. (1999). Myelination and organization of the frontal white matter in children: A diffusion tensor MRI study. Neuroreport, 10, 2817–2821.Google Scholar
Lehtinen, S.S., Huuskonen, U.E., Harila-Saari, A.H., Tolonen, U., Vainionpaa, L.K., & Lanning, B.M. (2002). Motor nervous system impairment persists in long-term survivors of childhood acute lymphoblastic leukemia. Cancer, 94, 2466–2473.Google Scholar
Lesnik, P.G., Ciesielski, K.T., Hart, B.L., Benzel, E.C., & Sanders, J.A. (1998). Evidence for cerebellar-frontal subsystem changes in children treated with intrathecal chemotherapy for leukemia—Enhanced data analysis using an effect size model. Archives of Neurology, 55, 1561–1568.Google Scholar
Madhyastha, S., Somayaji, S.N., Rao, M.S., Nalini, K., & Bairy, K.L. (2002). Hippocampal brain amines in methotrexate-induced learning and memory deficit. Canadian Journal of Physiology and Pharmacology, 80, 1076–1084.Google Scholar
Meadows, A.T., Gordon J., Massari D.J., Littman P., Fergusson J., & Moss K. (1981). Declines in IQ scores and cognitive dysfunctions in children with acute lymphocytic leukaemia treated with cranial irradiation. Lancet, 318, 1015–1018.Google Scholar
Miall, R.C., Reckess, G.Z., & Imamizu, H. (2001). The cerebellum coordinates eye and hand tracking movements. Nature Neuroscience, 4, 638–644.Google Scholar
Moleski, M. (2000). Neuropsychological, neuroanatomical, and neurophysiological consequences of CNS chemotherapy for acute lymphoblastic leukemia. Archives of Clinical Neuropsychology, 15, 603–630.Google Scholar
Mullenix, P.J., Kernan, W.J., Schunior, A., Howes, A., Waber, D.P., Sallan, S.E., & Tarbell, N.J. (1994). Interactions of steroid, methotrexate, and radiation determine neurotoxicity in an animal model to study therapy for childhood leukemia. Pediatric Research, 35, 171–178.Google Scholar
Muller, R.A., Kleinhans, N., Kemmotsu, N., Pierce, K., & Courchesne, E. (2003). Abnormal variability and distribution of functional maps in autism: An FMRI study of visuomotor learning. American Journal of Psychiatry, 160, 1847–1862.Google Scholar
Ochs, J., Mulhern, R., Fairclough, D., Parvey, L., Whitaker, J., Ch'ien, L., Mauer, A., & Simone, J. (1991). Comparison of neuropsychologic functioning and clinical indicators of neurotoxicity in long-term survivors of childhood leukemia given cranial radiation or parenteral methotrexate: A prospective study. Journal of Clinical Oncology, 9, 145–151.Google Scholar
Postma, T.J., Benard, B.A., Huijgens, P.C., Ossenkoppele, G.J., & Heimans, J.J. (1993). Long-term effects of vincristine on the peripheral nervous system. Journal of Neurooncology, 15, 23–27.Google Scholar
Pui, C.H., Mahmoud, H.H., Rivera, G.K., Hancock, M.L., Sandlund, J.T., Behm, F.G., Head, D.R., Relling, M.V., Ribeiro, R.C., Rubnitz, J.E., Kun, L.E., & Evans, W.E. (1998). Early intensification of intrathecal chemotherapy virtually eliminates central nervous system relapse in children with acute lymphoblastic leukemia. Blood, 92, 411–415.Google Scholar
Quinn, C.T., Griener, J.C., Bottiglieri, T., & Kamen, B.A. (1998). Methotrexate, homocysteine, and seizures. Journal of Clinical Oncology, 16, 393–394.Google Scholar
Reinders-Messelink, H.A., Schoemaker, M.M., Hofte, M., Goeken, L.N.H., Kingma, A., van den Briel, M.M., & Kamps, W.A. (1996). Fine motor and handwriting problems after treatment for childhood acute lymphoblastic leukemia. Medical and Pediatric Oncology, 27, 551–555.Google Scholar
Reinders-Messelink, H.A., Schoemaker, M.M., Snijders, T.A.B., Goeken, L.N.H., van den Briel, M.M., Bokkerink, J.P.M., & Kamps, W.A. (1999). Motor performance of children during treatment for acute lymphoblastic leukemia. Medical and Pediatric Oncology, 33, 545–550.Google Scholar
Reinders-Messelink, H.A., Schoemaker, M.M., Snijders, T.A.B., Goeken, L.N.H., Bokkerink, J.P.M., & Kamps, W.A. (2001). Analysis of handwriting of children during treatment for acute lymphoblastic leukemia. Medical and Pediatric Oncology, 37, 393–399.Google Scholar
Richer, F., Chouinard, M.J., & Rouleau, I. (1999). Frontal lesions impair the attentional control of movements during motor learning. Neuropsychologia, 37, 1427–1435.Google Scholar
Shuper, A., Stark, B., Kornreich, L., Cohen, I.J., Aviner, S., Steinmetz, A., Stein, J., Goshen, Y., & Yaniv, I. (2000). Methotrexate treatment protocols and the central nervous system: Significant cure with significant neurotoxicity. Journal of Child Neurology, 15, 573–580.Google Scholar
Surtees, R., Clelland, J., & Hann, I. (1998). Demyelination and single-carbon transfer pathway metabolites during the treatment of acute lymphoblastic leukemia: CSF studies. Journal of Clinical Oncology, 16, 1505–1511.Google Scholar
Tournade, M.F., Com-Nougue, C., de Kraker, J., Ludwig, R., Rey, A., Burgers, J.M., Sandstedt, B., Godzinski, J., Carli, M., Potter, R., & Zucker, J.M. (2001). Optimal duration of preoperative therapy in unilateral and nonmetastatic Wilms' tumor in children older than 6 months: Results of the Ninth International Society of Pediatric Oncology Wilms' tumor trial and study. Journal of Clinical Oncology, 19, 488–500.Google Scholar
Touwen, B.C.L. (1979). Examination of the child with minor neurological dysfunction. Clinics in Developmental Medicine (2nd ed.), Vol. 71. London: Heineman.
Tubergen, D.G., Gilchrist, G.S., O'Brien, R.T., Coccia, P.F., Sather, H.N., Waskerwitz, M.J., & Hammond, G.D. (1993). Prevention of CNS disease in intermediate-risk acute lymphoblastic leukemia: Comparison of cranial radiation and intrathecal methotrexate and the importance of systemic therapy: A Childrens Cancer Group report. Journal of Clinical Oncology, 11, 520–526.Google Scholar
Uitenbroek, D.G. (2003). SISA Bonferroni. Southampton, UK: D.G. Uitenbroek. Retrieved July 01, 2004, from the World Wide Web: http://home.clara.net/sisa/bonfer.htm
Vainionpaa, L. (1993). Clinical neurological findings of children with acute lymphoblastic-leukemia at diagnosis and during treatment. European Journal of Pediatrics, 152, 115–119.Google Scholar
Vainionpaa, L., Kovala, T., Tolonen, U., & Lanning, M. (1997). Chemotherapy for acute lymphoblastic leukemia may cause subtle changes of the spinal cord detectable by somatosensory evoked potentials. Medical and Pediatric Oncology, 28, 41–47.Google Scholar
Van Gool, S.W., Van Kerschaver, E., Brock, P., Pottel, H., Hulstaert, F., Vanmechelen, E., Uyttebroeck, A., Van De Voorde, A., & Vanderstichele, H. (2000). Disease- and treatment-related elevation of the neurodegenerative marker tau in children with hematological malignancies. Leukemia, 14, 2076–2084.Google Scholar
Veerman, A.J.P., Hahlen, K., Kamps, W.A., van Leeuwen, E.F., De Vaan, G.A., Solbu, G., Suciu, S., van Wering, E.R., & van der Does-Van den Berg, A. (1996). High cure rate with a moderately intensive treatment regimen in non-high-risk childhood acute lymphoblastic leukemia. Results of protocol ALL VI from the Dutch Childhood Leukemia Study Group. Journal of Clinical Oncology, 14, 911–918.Google Scholar
Verstappen, C.C.P., Heimans, J.J., Hoekman, K., & Postma, T.J. (2003). Neurotoxic complications of chemotherapy in patients with cancer—Clinical signs and optimal management. Drugs, 63, 1549–1563.Google Scholar
Vezmar, S., Becker, A., Bode, U., & Jaehde, U. (2003). Biochemical and clinical aspects of methotrexate neurotoxicity. Chemotherapy, 49, 92–104.CrossRefGoogle Scholar
Von der Weid, N., Mosimann, I., Hirt, A., Wacker, P., Nenadov, B.M., Imbach, P., Caflisch, U., Niggli, F., Feldges, A., & Wagner, H.P. (2003). Intellectual outcome in children and adolescents with acute lymphoblastic leukaemia treated with chemotherapy alone: Age- and sex-related differences. European Journal of Cancer, 39, 359–365.Google Scholar
Waber, D.P., Tarbell, N.J., Kahn, C.M., Gelber, R.D., & Sallan, S.E. (1992). The relationship of sex and treatment modality to neuropsychologic outcome in childhood acute lymphoblastic leukemia. Journal of Clinical Oncology, 10, 810–817.Google Scholar
Wise, S.P., Boussaoud, D., Johnson, P.B., & Caminiti, R. (1997). Premotor and parietal cortex: Corticocortical connectivity and combinatorial computations. Annual Review of Neuroscience, 20, 25–42.Google Scholar
Wright, M.J., Halton, J.M., Martin, R.F., & Barr, R.D. (1998). Long-term gross motor performance following treatment for acute lymphoblastic leukemia. Medical and Pediatric Oncology, 31, 86–90.Google Scholar