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Journal of Neuro-Oncology

, Volume 125, Issue 1, pp 9–21 | Cite as

A systematic review of cognitive performance in patients with childhood craniopharyngioma

  • Jale ÖzyurtEmail author
  • Hermann L. Müller
  • Christiane M. Thiel
Topic Review

Abstract

Craniopharyngiomas are rare brain tumors of the sellar/suprasellar region, often adversely affecting patients’ physical and psychosocial functioning. Until a few years ago, knowledge on cognitive deficits in craniopharyngioma patients was based on little valid evidence, with considerable inconsistencies across studies. Findings from recent research, with partly larger sample sizes, add to existing evidence to provide a more clear and reliable picture. The current review aims to summarize and systemize current findings on cognitive deficits in childhood craniopharyngioma, taking account of patient- and treatment-related variables where possible. Those studies were included that reported results of childhood craniopharyngioma patients tested with formalized neuropsychological tests (irrespective of their age at study, group size ≥10). A systematic assignment of test results to subcomponents of broader cognitive domains (e.g. to specific memory systems and processes) allows for a first comprehensive overview of patterns of spared and impaired cognitive functions. We show that episodic memory recall in particular is impaired, largely sparing other memory components. In accordance with recent knowledge on mammillary function, patients with hypothalamic involvement appear to be at particular risk. Deficits in higher cognitive processes, relying on the integrity of the prefrontal cortex and its subcortical pathways, may also occur, but results are still inconsistent. To gain deeper insight into the pattern of deficits and their association with patient- and treatment-related variables, further multi-site research with larger cohorts is needed.

Keywords

Brain tumors Cognitive Hypothalamus Craniopharyngioma Dysexecutive Memory 

Notes

Compliance with ethical standards

Conflict of interest

The authors have no conflicts of interest to disclose.

Financial disclosure

The authors have no financial relationships relevant to this article to disclose.

Funding source

German Childhood Cancer Foundation (DKS 2014.13). The German Childhood Cancer Foundation as the funding source was not involved in the study design; collection, analysis, and interpretation of data; the writing of the report; and the decision to submit the paper for publication.

Supplementary material

11060_2015_1885_MOESM1_ESM.docx (68 kb)
Supplementary material 1 (DOCX 68 kb)
11060_2015_1885_MOESM2_ESM.docx (49 kb)
Supplementary material 2 (DOCX 48 kb)

References

  1. 1.
    Muller HL (2010) Childhood craniopharyngioma–current concepts in diagnosis, therapy and follow-up. Nat Rev Endocrinol 6(11):609–618. doi: 10.1038/nrendo.2010.168 CrossRefPubMedGoogle Scholar
  2. 2.
    Zada G, Kintz N, Pulido M, Amezcua L (2013) Prevalence of neurobehavioral, social, and emotional dysfunction in patients treated for childhood craniopharyngioma: a systematic literature review. PLoS One 8(11):e76562. doi: 10.1371/journal.pone.0076562 PubMedCentralCrossRefPubMedGoogle Scholar
  3. 3.
    Laffond C, Dellatolas G, Alapetite C, Puget S, Grill J, Habrand JL, Doz F, Chevignard M (2012) Quality-of-life, mood and executive functioning after childhood craniopharyngioma treated with surgery and proton beam therapy. Brain Inj 26(3):270–281. doi: 10.3109/02699052.2011.648709 CrossRefPubMedGoogle Scholar
  4. 4.
    Muller HL, Bueb K, Bartels U, Roth C, Harz K, Graf N, Korinthenberg R, Bettendorf M, Kuhl J, Gutjahr P, Sorensen N, Calaminus G (2001) Obesity after childhood craniopharyngioma–German multicenter study on pre-operative risk factors and quality of life. Klin Padiatr 213(4):244–249. doi: 10.1055/s-2001-16855 CrossRefPubMedGoogle Scholar
  5. 5.
    Muller HL (2013) Paediatrics: surgical strategy and quality of life in craniopharyngioma. Nat Rev Endocrinol 9(8):447–449. doi: 10.1038/nrendo.2013.125 CrossRefPubMedGoogle Scholar
  6. 6.
    Muller HL, Bruhnken G, Emser A, Faldum A, Etavard-Gorris N, Gebhardt U, Kolb R, Sorensen N (2005) Longitudinal study on quality of life in 102 survivors of childhood craniopharyngioma. Child’s Nerv Syst 21(11):975–980. doi: 10.1007/s00381-004-1124-y CrossRefGoogle Scholar
  7. 7.
    Merchant TE, Kiehna EN, Sanford RA, Mulhern RK, Thompson SJ, Wilson MW, Lustig RH, Kun LE (2002) Craniopharyngioma: the St. Jude Children’s Research Hospital experience 1984–2001. Int J Radiat Oncol Biol Phys 53(3):533–542CrossRefPubMedGoogle Scholar
  8. 8.
    Poretti A, Grotzer MA, Ribi K, Schonle E, Boltshauser E (2004) Outcome of craniopharyngioma in children: long-term complications and quality of life. Dev Med Child Neurol 46(4):220–229CrossRefPubMedGoogle Scholar
  9. 9.
    Netson KL, Conklin HM, Wu S, Xiong X, Merchant TE (2013) Longitudinal investigation of adaptive functioning following conformal irradiation for pediatric craniopharyngioma and low-grade glioma. Int J Radiat Oncol Biol Phys 85(5):1301–1306. doi: 10.1016/j.ijrobp.2012.10.031 PubMedCentralCrossRefPubMedGoogle Scholar
  10. 10.
    Merchant TE, Kiehna EN, Kun LE, Mulhern RK, Li C, Xiong X, Boop FA, Sanford RA (2006) Phase II trial of conformal radiation therapy for pediatric patients with craniopharyngioma and correlation of surgical factors and radiation dosimetry with change in cognitive function. J Neurosurg 104(2 Suppl):94–102. doi: 10.3171/ped.2006.104.2.5 PubMedGoogle Scholar
  11. 11.
    Pedreira CC, Stargatt R, Maroulis H, Rosenfeld J, Maixner W, Warne GL, Zacharin MR (2006) Health related quality of life and psychological outcome in patients treated for craniopharyngioma in childhood. J Pediatr Endocrinol Metab 19(1):15–24CrossRefPubMedGoogle Scholar
  12. 12.
    Galatzer A, Nofar E, Beit-Halachmi N, Aran O, Shalit M, Roitman A, Laron Z (1981) Intellectual and psychosocial functions of children, adolescents and young adults before and after operation for craniopharyngioma. Child Care Health Dev 7(6):307–316CrossRefPubMedGoogle Scholar
  13. 13.
    Eiser C (1981) Psychological sequelae of brain tumours in childhood: a retrospective study. Br J Clin Psychol 20(Pt 1):35–38CrossRefPubMedGoogle Scholar
  14. 14.
    Anderson CA, Wilkening GN, Filley CM, Reardon MS, Kleinschmidt-DeMasters BK (1997) Neurobehavioral outcome in pediatric craniopharyngioma. Pediatr Neurosurg 26(5):255–260CrossRefPubMedGoogle Scholar
  15. 15.
    Schubert T, Trippel M, Tacke U, van Velthoven V, Gumpp V, Bartelt S, Ostertag C, Nikkhah G (2009) Neurosurgical treatment strategies in childhood craniopharyngiomas: is less more? Child’s Nerv Syst 25(11):1419–1427. doi: 10.1007/s00381-009-0978-4 CrossRefGoogle Scholar
  16. 16.
    Pierre-Kahn A, Recassens C, Pinto G, Thalassinos C, Chokron S, Soubervielle JC, Brauner R, Zerah M, Sainte Rose C (2005) Social and psycho-intellectual outcome following radical removal of craniopharyngiomas in childhood. A prospective series. Child’s Nerv Syst 21(8–9):817–824. doi: 10.1007/s00381-005-1205-6 CrossRefGoogle Scholar
  17. 17.
    Thompson D, Phipps K, Hayward R (2005) Craniopharyngioma in childhood: our evidence-based approach to management. Child’s Nerv Syst 21(8–9):660–668. doi: 10.1007/s00381-005-1210-9 CrossRefGoogle Scholar
  18. 18.
    Mottolese C, Szathmari A, Berlier P, Hermier M (2005) Craniopharyngiomas: our experience in Lyon. Child’s Nerv Syst 21(8–9):790–798. doi: 10.1007/s00381-005-1242-1 CrossRefGoogle Scholar
  19. 19.
    Kalapurakal JA, Goldman S, Hsieh YC, Tomita T, Marymont MH (2003) Clinical outcome in children with craniopharyngioma treated with primary surgery and radiotherapy deferred until relapse. Med Pediatr Oncol 40(4):214–218. doi: 10.1002/mpo.10247 CrossRefPubMedGoogle Scholar
  20. 20.
    Colangelo M, Ambrosio A, Ambrosio C (1990) Neurological and behavioral sequelae following different approaches to craniopharyngioma. Child’s Nerv Syst 6(7):379–382CrossRefGoogle Scholar
  21. 21.
    Carpentieri SC, Waber DP, Scott RM, Goumnerova LC, Kieran MW, LE Cohen, Kim F, Billett AL, Tarbell NJ, Pomeroy SL (2001) Memory deficits among children with craniopharyngiomas. Neurosurg 49(5):1053–1057 (discussion 1057–1058) Google Scholar
  22. 22.
    Cavazzuti V, Fischer EG, Welch K, Belli JA, Winston KR (1983) Neurological and psychophysiological sequelae following different treatments of craniopharyngioma in children. J Neurosurg 59(3):409–417. doi: 10.3171/jns.1983.59.3.0409 CrossRefPubMedGoogle Scholar
  23. 23.
    Kiehna EN, Mulhern RK, Li C, Xiong X, Merchant TE (2006) Changes in attentional performance of children and young adults with localized primary brain tumors after conformal radiation therapy. J Clin Oncol 24(33):5283–5290. doi: 10.1200/jco.2005.03.8547 CrossRefPubMedGoogle Scholar
  24. 24.
    Waber DP, Pomeroy SL, Chiverton AM, Kieran MW, Scott RM, Goumnerova LC, Rivkin MJ (2006) Everyday cognitive function after craniopharyngioma in childhood. Pediatr Neurol 34(1):13–19. doi: 10.1016/j.pediatrneurol.2005.06.002 CrossRefPubMedGoogle Scholar
  25. 25.
    Riva D, Pantaleoni C, Devoti M, Saletti V, Nichelli F, Giorgi C (1998) Late neuropsychological and behavioural outcome of children surgically treated for craniopharyngioma. Child’s Nerv Syst 14(4–5):179–184CrossRefGoogle Scholar
  26. 26.
    Bawden HN, Salisbury S, Eskes G, Morehouse R (2009) Neuropsychological functioning following craniopharyngioma removal. J Clin Exp Neuropsychol 31(1):140–144. doi: 10.1080/13803390802064599 CrossRefPubMedGoogle Scholar
  27. 27.
    Ozyurt J, Thiel CM, Lorenzen A, Gebhardt U, Calaminus G, Warmuth-Metz M, Muller HL (2014) Neuropsychological outcome in patients with childhood craniopharyngioma and hypothalamic involvement. J Pediatr 164(4):876–881. doi: 10.1016/j.jpeds.2013.12.010 e874 CrossRefPubMedGoogle Scholar
  28. 28.
    Fjalldal S, Holmer H, Rylander L, Elfving M, Ekman B, Osterberg K, Erfurth EM (2013) Hypothalamic involvement predicts cognitive performance and psychosocial health in long-term survivors of childhood craniopharyngioma. J Clin Endocrinol Metab 98(8):3253–3262. doi: 10.1210/jc.2013-2000 CrossRefPubMedGoogle Scholar
  29. 29.
    Di Pinto M, Conklin HM, Li C, Merchant TE (2012) Learning and memory following conformal radiation therapy for pediatric craniopharyngioma and low-grade glioma. Int J Radiat Oncol Biol Phys 84(3):e363–369. doi: 10.1016/j.ijrobp.2012.03.066 PubMedCentralCrossRefPubMedGoogle Scholar
  30. 30.
    de Vile CJ, Grant DB, Hayward RD, Kendall BE, Neville BG, Stanhope R (1996) Obesity in childhood craniopharyngioma: relation to post-operative hypothalamic damage shown by magnetic resonance imaging. J Clin Endocrinol Metab 81(7):2734–2737. doi: 10.1210/jcem.81.7.8675604 PubMedGoogle Scholar
  31. 31.
    Puget S, Garnett M, Wray A, Grill J, Habrand JL, Bodaert N, Zerah M, Bezerra M, Renier D, Pierre-Kahn A, Sainte-Rose C (2007) Pediatric craniopharyngiomas: classification and treatment according to the degree of hypothalamic involvement. J Neurosurg 106(1 Suppl):3–12. doi: 10.3171/ped.2007.106.1.3 PubMedGoogle Scholar
  32. 32.
    Liberati A, Altman DG, Tetzlaff J, Mulrow C, Gotzsche PC, Ioannidis JP, Clarke M, Devereaux PJ, Kleijnen J, Moher D (2009) The PRISMA statement for reporting systematic reviews and meta-analyses of studies that evaluate health care interventions: explanation and elaboration. PLoS Med 6(7):e1000100. doi: 10.1371/journal.pmed.1000100 PubMedCentralCrossRefPubMedGoogle Scholar
  33. 33.
    Ondruch A, Maryniak A, Kropiwnicki T, Roszkowski M, Daszkiewicz P (2011) Cognitive and social functioning in children and adolescents after the removal of craniopharyngioma. Child’s Nerv Syst 27(3):391–397. doi: 10.1007/s00381-010-1301-0 CrossRefGoogle Scholar
  34. 34.
    Strauss E, Sherman EMS, Spreen O (2006) A compendium of neuropsychological tests. Oxford University Press, Oxford, New YorkGoogle Scholar
  35. 35.
    Hoffman HJ, De Silva M, Humphreys RP, Drake JM, Smith ML, Blaser SI (1992) Aggressive surgical management of craniopharyngiomas in children. J Neurosurg 76(1):47–52. doi: 10.3171/jns.1992.76.1.0047 CrossRefPubMedGoogle Scholar
  36. 36.
    Flick T, Michel M (1986) Rehabilitation of young craniopharyngioma patients. Rehabil (Stuttg) 25(2):45–52Google Scholar
  37. 37.
    Clopper RR, Meyer WJ 3rd, Udvarhelyi GB, Money J, Aarabi B, Mulvihill JJ, Piasio M (1977) Postsurgical IQ and behavioral data on twenty patients with a history of childhood craniopharyngioma. Psychoneuroendocrinology 2(4):365–372CrossRefPubMedGoogle Scholar
  38. 38.
    Dhellemmes P, Vinchon M (2006) Radical resection for craniopharyngiomas in children: surgical technique and clinical results. J Pediatr Endocrinol Metab 19(Suppl 1):329–335PubMedGoogle Scholar
  39. 39.
    Aggleton JP (2012) Multiple anatomical systems embedded within the primate medial temporal lobe: implications for hippocampal function. Neurosci Biobehav Rev 36(7):1579–1596. doi: 10.1016/j.neubiorev.2011.09.005 CrossRefPubMedGoogle Scholar
  40. 40.
    Vann SD (2010) Re-evaluating the role of the mammillary bodies in memory. Neuropsychologia 48(8):2316–2327. doi: 10.1016/j.neuropsychologia.2009.10.019 CrossRefPubMedGoogle Scholar
  41. 41.
    Tsivilis D, Vann SD, Denby C, Roberts N, Mayes AR, Montaldi D, Aggleton JP (2008) A disproportionate role for the fornix and mammillary bodies in recall versus recognition memory. Nat Neurosci 11(7):834–842. doi: 10.1038/nn.2149 CrossRefPubMedGoogle Scholar
  42. 42.
    Muller HL (2008) Childhood craniopharyngioma. Recent advances in diagnosis, treatment and follow-up. Horm Res 69(4):193–202. doi: 10.1159/000113019 CrossRefPubMedGoogle Scholar
  43. 43.
    Garnett MR, Puget S, Grill J, Sainte-Rose C (2007) Craniopharyngioma. Orphanet J rare Dis 2:18. doi: 10.1186/1750-1172-2-18 PubMedCentralCrossRefPubMedGoogle Scholar
  44. 44.
    Lemaire JJ, Frew AJ, McArthur D, Gorgulho AA, Alger JR, Salomon N, Chen C, Behnke EJ, De Salles AA (2011) White matter connectivity of human hypothalamus. Brain Res 1371:43–64. doi: 10.1016/j.brainres.2010.11.072 CrossRefPubMedGoogle Scholar
  45. 45.
    Aggleton JP, Dumont JR, Warburton EC (2011) Unraveling the contributions of the diencephalon to recognition memory: a review. Learn Mem 18(6):384–400. doi: 10.1101/lm.1884611 PubMedCentralCrossRefPubMedGoogle Scholar
  46. 46.
    Ellenberg L, Liu Q, Gioia G, Yasui Y, Packer RJ, Mertens A, Donaldson SS, Stovall M, Kadan-Lottick N, Armstrong G, Robison LL, Zeltzer LK (2009) Neurocognitive status in long-term survivors of childhood CNS malignancies: a report from the childhood cancer survivor study. Neuropsychology 23(6):705–717. doi: 10.1037/a0016674 PubMedCentralCrossRefPubMedGoogle Scholar
  47. 47.
    Turken A, Whitfield-Gabrieli S, Bammer R, Baldo JV, Dronkers NF, Gabrieli JD (2008) Cognitive processing speed and the structure of white matter pathways: convergent evidence from normal variation and lesion studies. NeuroImage 42(2):1032–1044. doi: 10.1016/j.neuroimage.2008.03.057 PubMedCentralCrossRefPubMedGoogle Scholar
  48. 48.
    Batista S, Zivadinov R, Hoogs M, Bergsland N, Heininen-Brown M, Dwyer MG, Weinstock-Guttman B, Benedict RH (2012) Basal ganglia, thalamus and neocortical atrophy predicting slowed cognitive processing in multiple sclerosis. J Neurol 259(1):139–146. doi: 10.1007/s00415-011-6147-1 CrossRefPubMedGoogle Scholar
  49. 49.
    Puget S (2012) Treatment strategies in childhood craniopharyngioma. Front Endocrinol 3:64. doi: 10.3389/fendo.2012.00064 CrossRefGoogle Scholar
  50. 50.
    Jalali R, Mallick I, Dutta D, Goswami S, Gupta T, Munshi A, Deshpande D, Sarin R (2010) Factors influencing neurocognitive outcomes in young patients with benign and low-grade brain tumors treated with stereotactic conformal radiotherapy. Int J Radiat Oncol Biol Phys 77(4):974–979. doi: 10.1016/j.ijrobp.2009.06.025 CrossRefPubMedGoogle Scholar
  51. 51.
    Muller HL (2013) Childhood craniopharyngioma. Pituitary 16(1):56–67. doi: 10.1007/s11102-012-0401-0 CrossRefPubMedGoogle Scholar
  52. 52.
    Ozyurt J, Lorenzen A, Gebhardt U, Warmuth-Metz M, Muller HL, Thiel CM (2014) Remote effects of hypothalamic lesions in the prefrontal cortex of craniopharygioma patients. Neurobiol Learn Mem. doi: 10.1016/j.nlm.2014.03.007 PubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2015

Authors and Affiliations

  • Jale Özyurt
    • 1
    Email author
  • Hermann L. Müller
    • 2
  • Christiane M. Thiel
    • 1
    • 3
    • 4
  1. 1.Biological Psychology Lab, Department of Psychology, European Medical SchoolCarl von Ossietzky UniversitätOldenburgGermany
  2. 2.Department of Pediatrics and Pediatric Hematology and Oncology, Zentrum für Kinder-und Jugendmedizin, Klinikum OldenburgMedical Campus University OldenburgOldenburgGermany
  3. 3.Research Center Neurosensory ScienceCarl von Ossietzky UniversitätOldenburgGermany
  4. 4.Cluster of Excellence “Hearing4all”Carl von Ossietzky Universität OldenburgOldenburgGermany

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