Neuropsychological functioning following surgery for pediatric low-grade glioma: a prospective longitudinal study

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  • 1 Department of Pediatrics, Section of Psychology, Baylor College of Medicine;
  • 2 Dan L. Duncan Institute for Clinical and Translational Research, Baylor College of Medicine;
  • 4 Department of Pediatrics, Section of Hematology Oncology, Baylor College of Medicine;
  • 5 Department of Neurosurgery, Division of Pediatric Neurosurgery, Baylor College of Medicine; and
  • 3 Rice University, Houston, Texas
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OBJECTIVE

High survival rates have led to an increased emphasis on the functional outcomes of children diagnosed with low-grade glioma. Most outcomes research has focused on risks associated with radiotherapy, but less is known about neuropsychological risks for patients treated with surgery alone. Here, the authors sought to examine the neuropsychological trajectories of children diagnosed with a low-grade glioma and monitored up to 6 years postsurgery. Secondarily, they explored demographic and clinical predictors of neuropsychological performance.

METHODS

The neuropsychological functioning of 32 patients (median age at diagnosis 10.0 years) was prospectively assessed annually for up to 6 years after surgery (median days from surgery at baseline = 72). Tumor location was predominately supratentorial (65.6%). A combination of performance-based and parent-reported measures was used to assess intelligence, memory, executive functioning, and fine motor control in all patients.

RESULTS

Binomial tests at the postoperative baseline revealed that the proportion of children falling below the average range (< 16th percentile) was significantly higher than the rate expected among healthy peers on measures of verbal memory, processing speed, executive functioning, and fine motor control (p < 0.05). Even so, linear mixed models indicated that neuropsychological functioning at the postoperative baseline did not significantly change over time for up to 6 years after surgery across all domains. A larger tumor size was associated with a slower reaction time (p < 0.01). A supratentorial tumor location and history of seizures were associated with more parent-reported executive difficulties (p < 0.01).

CONCLUSIONS

While radiotherapy is a known risk factor for neuropsychological deficits in pediatric brain tumor patients, findings in this study indicate that children treated for low-grade glioma with surgery alone (without radiotherapy or chemotherapy) remain susceptible to difficulties with memory, executive functioning, and motor functioning that persist over time. Over half of the children in the study sample required school support services to address neuropsychological weaknesses. Although low-grade glioma is often conceptualized as a benign tumor, children treated for this lesion require ongoing monitoring and intervention to address neuropsychological weaknesses resulting from the tumor itself as well as the surgery.

ABBREVIATIONS BRIEF = Behavior Rating Inventory of Executive Function; CPT = Continuous Performance Test; D-KEFS = Delis-Kaplan Executive Function System; FSIQ = Full Scale IQ; LGG = low-grade glioma; PRI = Perceptual Reasoning Index; PSI = Processing Speed Index; VCI = Verbal Comprehension Index; WISC-V = Wechsler Intelligence Scale for Children, Fifth Edition; WMI = Working Memory Index.

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Contributor Notes

Correspondence Lisa S. Kahalley: Texas Children’s Hospital, Houston, TX. kahalley@bcm.edu.

INCLUDE WHEN CITING Published online December 6, 2019; DOI: 10.3171/2019.9.PEDS19357.

Disclosures This work was supported in part by the National Cancer Institute (R01CA187202 and K07CA157923) and the Texas Children’s Hospital Pediatric Pilot Research Fund (Principal Investigator: Lisa Kahalley). Additional support was provided by the National Cancer Institute (R01CA221197, Principal Investigators: Lisa Kahalley and Elisabeth Wilde). Dr. Minard is a statistical reviewer for the journal Chest.

  • 1

    Bandopadhayay P, Bergthold G, London WB, Goumnerova LC, Morales La Madrid A, Marcus KJ, : Long-term outcome of 4,040 children diagnosed with pediatric low-grade gliomas: an analysis of the Surveillance Epidemiology and End Results (SEER) database. Pediatr Blood Cancer 61:11731179, 2014

    • Search Google Scholar
    • Export Citation
  • 2

    Beebe DW, Ris MD, Armstrong FD, Fontanesi J, Mulhern R, Holmes E, : Cognitive and adaptive outcome in low-grade pediatric cerebellar astrocytomas: evidence of diminished cognitive and adaptive functioning in National Collaborative Research Studies (CCG 9891/POG 9130). J Clin Oncol 23:51985204, 2005

    • Search Google Scholar
    • Export Citation
  • 3

    Beery KE, Beery NA: Beery VMI: The Beery-Buktenica Developmental Test of Visual-Motor Integration With Supplemental Developmental Tests of Visual Perception and Motor Coordination: And, Stepping Stones Age Norms From Birth to Age Six. Administration, Scoring, and Teaching Manual. San Antonio: PsychCorp, 2010

    • Search Google Scholar
    • Export Citation
  • 4

    Berger A, Sadeh M, Tzur G, Shuper A, Kornreich L, Inbar D, : Task switching after cerebellar damage. Neuropsychology 19:362370, 2005

  • 5

    Conners KC: Conners’ Continuous Performance Test II. San Antonio: Pearson Corporation, 2004

  • 6

    Conners KC: Conners’ Kiddie Continuous Performance Test. North Tonawanda, NY: Multi-Health Systems, 2006

  • 7

    Delis DC, Kaplan E, Kramer JH: Delis-Kaplan Executive Function System (D-KEFS). San Antonio: The Psychological Corporation, 2001

  • 8

    Delis DC, Kramer JH, Kaplan E, Ober BA: California Verbal Learning Test, Children’s Version. San Antonio: Psychological Corporation, 1994

    • Search Google Scholar
    • Export Citation
  • 9

    Delis DC, Kramer JH, Kaplan E, Ober BA: California Verbal Learning Test, Second Edition (CVLT-II). San Antonio: Psychological Corporation, 2000

    • Search Google Scholar
    • Export Citation
  • 10

    Duffau H, Capelle L, Denvil D, Sichez N, Gatignol P, Lopes M, : Functional recovery after surgical resection of low grade gliomas in eloquent brain: hypothesis of brain compensation. J Neurol Neurosurg Psychiatry 74:901907, 2003

    • Search Google Scholar
    • Export Citation
  • 11

    Gioia G, Isquith P, Guy S, Kenworthy L: Behavior Rating Inventory of Executive Function. Odessa, FL: Psychological Assessment Resources, 2000

    • Search Google Scholar
    • Export Citation
  • 12

    Heitzer AM, Ashford JM, Hastings C, Liu APY, Wu S, Bass JK, : Neuropsychological outcomes of patients with low-grade glioma diagnosed during the first year of life. J Neurooncol 141:413420, 2019

    • Search Google Scholar
    • Export Citation
  • 13

    Iddon JL, Morgan DJ, Loveday C, Sahakian BJ, Pickard JD: Neuropsychological profile of young adults with spina bifida with or without hydrocephalus. J Neurol Neurosurg Psychiatry 75:11121118, 2004

    • Search Google Scholar
    • Export Citation
  • 14

    Korkman M, Kirk U, Kemp S: NEPSY—Second Edition (NEPSY-II). San Antonio: Harcourt Assessment, 2007

  • 15

    Lafayette Instruments: Grooved Pegboard Test User Instructions. Lafayette, IN: Lafayette Instrument Company Inc, 1989

  • 16

    Levisohn L, Cronin-Golomb A, Schmahmann JD: Neuropsychological consequences of cerebellar tumour resection in children: cerebellar cognitive affective syndrome in a paediatric population. Brain 123:10411050, 2000

    • Search Google Scholar
    • Export Citation
  • 17

    LoGalbo A, Sawrie S, Roth DL, Kuzniecky R, Knowlton R, Faught E, : Verbal memory outcome in patients with normal preoperative verbal memory and left mesial temporal sclerosis. Epilepsy Behav 6:337341, 2005

    • Search Google Scholar
    • Export Citation
  • 18

    Luu TM, Ment L, Allan W, Schneider K, Vohr BR: Executive and memory function in adolescents born very preterm. Pediatrics 127:e639e646, 2011

    • Search Google Scholar
    • Export Citation
  • 19

    Merchant TE, Conklin HM, Wu S, Lustig RH, Xiong X: Late effects of conformal radiation therapy for pediatric patients with low-grade glioma: prospective evaluation of cognitive, endocrine, and hearing deficits. J Clin Oncol 27:36913697, 2009

    • Search Google Scholar
    • Export Citation
  • 20

    Merchant TE, Lee H, Zhu J, Xiong X, Wheeler G, Phipps S, : The effects of hydrocephalus on intelligence quotient in children with localized infratentorial ependymoma before and after focal radiation therapy. J Neurosurg 101 (2 Suppl):159168, 2004

    • Search Google Scholar
    • Export Citation
  • 21

    Mulhern RK, Butler RW: Neurocognitive sequelae of childhood cancers and their treatment. Pediatr Rehabil 7:116, 2004

  • 22

    Netson KL, Conklin HM, Wu S, Xiong X, Merchant TE: A 5-year investigation of children’s adaptive functioning following conformal radiation therapy for localized ependymoma. Int J Radiat Oncol Biol Phys 84:217223.e1, 2012

    • Search Google Scholar
    • Export Citation
  • 23

    Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, Barnholtz-Sloan JS: CBTRUS statistical report: primary brain and other central nervous system tumors diagnosed in the United States in 2011–2015. Neuro Oncol 20 (Suppl 4):iv1iv86, 2018

    • Search Google Scholar
    • Export Citation
  • 24

    Pletschko T, Felnhofer A, Lamplmair D, Dorfer C, Czech T, Chocholous M, : Cerebellar pilocytic astrocytoma in childhood: Investigating the long-term impact of surgery on cognitive performance and functional outcome. Dev Neurorehabil 21:415422, 2018

    • Search Google Scholar
    • Export Citation
  • 25

    Reid R, Riccio CA, Kessler RH, Dupaul GJ, Power TJ, Anastopoulos AD, : Gender and ethnic differences in ADHD as assessed by behavior ratings. J Emot Behav Disord 8:3848, 2000

    • Search Google Scholar
    • Export Citation
  • 26

    Reimers TS, Ehrenfels S, Mortensen EL, Schmiegelow M, Sønderkaer S, Carstensen H, : Cognitive deficits in long-term survivors of childhood brain tumors: Identification of predictive factors. Med Pediatr Oncol 40:2634, 2003

    • Search Google Scholar
    • Export Citation
  • 27

    Ris MD, Beebe DW: Neurodevelopmental outcomes of children with low-grade gliomas. Dev Disabil Res Rev 14:196202, 2008

  • 28

    Ris MD, Beebe DW, Armstrong FD, Fontanesi J, Holmes E, Sanford RA, : Cognitive and adaptive outcome in extracerebellar low-grade brain tumors in children: a report from the Children’s Oncology Group. J Clin Oncol 26:47654770, 2008

    • Search Google Scholar
    • Export Citation
  • 29

    Roman MJ, Delis DC, Willerman L, Magulac M, Demadura TL, de la Peña JL, : Impact of pediatric traumatic brain injury on components of verbal memory. J Clin Exp Neuropsychol 20:245258, 1998

    • Search Google Scholar
    • Export Citation
  • 30

    Sabbagh MA, Xu F, Carlson SM, Moses LJ, Lee K: The development of executive functioning and theory of mind. A comparison of Chinese and U.S. preschoolers. Psychol Sci 17:7481, 2006

    • Search Google Scholar
    • Export Citation
  • 31

    Scheibel RS, Meyers CA, Levin VA: Cognitive dysfunction following surgery for intracerebral glioma: influence of histopathology, lesion location, and treatment. J Neurooncol 30:6169, 1996

    • Search Google Scholar
    • Export Citation
  • 32

    Sesma HW, Slomine BS, Ding R, McCarthy ML: Executive functioning in the first year after pediatric traumatic brain injury. Pediatrics 121:e1686e1695, 2008

    • Search Google Scholar
    • Export Citation
  • 33

    Sherman EM, Wiebe S, Fay-McClymont TB, Tellez-Zenteno J, Metcalfe A, Hernandez-Ronquillo L, : Neuropsychological outcomes after epilepsy surgery: systematic review and pooled estimates. Epilepsia 52:857869, 2011

    • Search Google Scholar
    • Export Citation
  • 34

    Tucha O, Smely C, Preier M, Lange KW: Cognitive deficits before treatment among patients with brain tumors. Neurosurgery 47:324334, 2000

    • Search Google Scholar
    • Export Citation
  • 35

    Turken A, Whitfield-Gabrieli S, Bammer R, Baldo JV, Dronkers NF, Gabrieli JDE: Cognitive processing speed and the structure of white matter pathways: convergent evidence from normal variation and lesion studies. Neuroimage 42:10321044, 2008

    • Search Google Scholar
    • Export Citation
  • 36

    Turner CD, Chordas CA, Liptak CC, Rey-Casserly C, Delaney BL, Ullrich NJ, : Medical, psychological, cognitive and educational late-effects in pediatric low-grade glioma survivors treated with surgery only. Pediatr Blood Cancer 53:417423, 2009

    • Search Google Scholar
    • Export Citation
  • 37

    Wechsler D: Wechsler Adult Intelligence Scale—Fourth Edition (WAIS–IV). San Antonio: Psychological Corporation, 2014

  • 38

    Wechsler D: Wechsler Intelligence Scale for Children—Fifth Edition (WISC-V). San Antonio: Psychological Corporation, 2014

  • 39

    Wechsler D: Wechsler Intelligence Scale for Children—Fourth Edition. San Antonio: The Psychological Corporation, 2003

  • 40

    Wechsler D: Wechsler Memory Scale—Fourth Edition (WMS–IV) Technical and Interpretive Manual. San Antonio: Pearson, 2009

  • 41

    Wechsler D: Wechsler Primary and Preschool Scale of Intelligence—Third Edition (WPPSI-III). San Antonio: Harcourt Assessment, 2002

  • 42

    Wechsler D, Coalson D, Raiford S: Wechsler Preschool and Primary Scale of Intelligence—Fourth Edition (WPPSI-IV). San Antonio: The Psychological Corporation, 2012

    • Search Google Scholar
    • Export Citation
  • 43

    Westmacott R, Askalan R, MacGregor D, Anderson P, Deveber G: Cognitive outcome following unilateral arterial ischaemic stroke in childhood: effects of age at stroke and lesion location. Dev Med Child Neurol 52:386393, 2010

    • Search Google Scholar
    • Export Citation
  • 44

    Wisoff JH, Sanford RA, Heier LA, Sposto R, Burger PC, Yates AJ, : Primary neurosurgery for pediatric low-grade gliomas: a prospective multi-institutional study from the Children’s Oncology Group. Neurosurgery 68:15481555, 2011

    • Search Google Scholar
    • Export Citation

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