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Language Impairment Associated With Arachnoid Cysts: Recovery After Surgical Treatment
Pediatric Neurology 46 (2012) 44e47
Contents lists available at ScienceDirect
Pediatric Neurology journal homepage: www.elsevier.com/locate/pnu
Case Report
Language Impairment Associated With Arachnoid Cysts: Recovery After Surgical Treatment Nicole Laporte BSc a, Anne De Volder MD, PhD a, Christine Bonnier MD, PhD a, Christian Raftopoulos MD, PhD b, Guillaume Sébire MD, PhD c, * a
Service de Neuropédiatrie, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Brussels, Belgium Service de Neurochirurgie, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Brussels, Belgium c Service de Neurologie Pédiatrique, Centre Hospitalier Universitaire de Sherbrooke, Faculté de Médecine, Université de Sherbrooke, Sherbrooke, Quebec, Canada b
article information
abstract
Article history: Received 23 May 2010 Accepted 3 October 2011
Supporting data from the literature, we observe that large arachnoid cysts may affect cognitive function. Neuropsychologic assessment plus magnetic resonance imaging allowed for documentation of associations between left temporal arachnoid cysts, language impairment, and other cognitive dysfunctions. Significant cognitive improvements were evident soon after cysto-peritoneal shunting. These observations reinforce the rationale for neuropsychologic assessments of patients with developmental delay and arachnoid cysts, and support the potential benefit of surgical decompression for arachnoid cysts associated with neurologic deficits, even if surgery is performed well after the occurrence of neurologic deficits. Ó 2012 Elsevier Inc. All rights reserved.
Introduction Most arachnoid cysts are congenital, likely arising by the anomalous splitting of the arachnoidal layer of the meninges [1-3]. They are usually discovered incidentally during neuroimaging of asymptomatic patients [1]. However, certain clinical manifestations related to arachnoid cysts were reported, such as headaches, enlargements of head circumference, temporal bulging, intracranial hypertension, and partial seizures [2-17]. Only a few studies have dealt with cognitive dysfunctions associated with arachnoid cysts in childhood [5-13]. We report on two patients with arachnoid cysts adjacent to the temporal pole. Both patients presented with developmental language impairment, and both patients exhibited a rapid and significant language improvement postoperatively. Patients and Methods We retrospectively studied two patients presenting with arachnoid cysts associated with cognitive impairment. Both children were admitted between 1997 and 2002 in the Department of Child Neurology and Department of Neurosurgery at the Cliniques Universitaires Saint-Luc (Université Catholique de Louvain, Brussels, Belgium). During this timeframe, no other patients with clinically symptomatic * Communications should be addressed to: Dr. Sébire; Service de Neurologie Pédiatrique; Centre Hospitalier Universitaire de Sherbrooke; Faculté de Médecine; Université de Sherbrooke; 3001 12ème Avenue Nord; Sherbrooke, Quebec J1H5N4, Canada. E-mail address: [email protected] 0887-8994/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.pediatrneurol.2011.10.001
arachnoid cysts were recruited. These two patients underwent serial clinical, neuroradiologic (1.5 T cranial magnetic resonance imaging in patients 1 and 2, and positron emission tomography, i.e., an [18F] fludeoxyglucose scan, in patient 1), and neuropsychologic and language assessments before and after neurosurgical treatment. We paid particular attention to cognitive outcomes, focusing on linguistic functions that were deficient before surgery. The durations of follow-up were 6 years for patient 1, and 18 months for patient 2. Psychometric investigations were performed using the Échelle d’Intelligence de Wechsler pour la Période Préscolaire et Primaire (or its revised form) and the Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition. Language assessment was performed using the Epreuves pour l’Examen du Language, the Batterie d’Evaluation Psycholinguistique, the Nouvelles Epreuves pour l’Examen du Language, the Batterie Language Oral-Language Ecrit-Attention, the Test de Vocabulaire Actif et Passif, the Evaluation des Aptitudes Syntaxiques, and the Epreuves de Compréhension Syntaxique Sémantique. Memory was measured with specific subtests of Korkman’s Developmental Neuropsychological Assessment, the Batterie pour l’Examen Psychologique de l’Enfant, the Figure de Rey, the Auditory Verbal Learning Test, and the Epreuves de Reconnaissance Verbale. Attention was measured according to the Test de Zazzo, i.e., the Test of Everyday Attention. School learning level was measured with the Tests Pédagogiques du Premier Cycle Primaire, the Epreuves d’Apprentissage Scolaire Primaire, the Lecture de Mots et Compréhension, and Le Poucet. Patient 1 This 6-year-old, right-handed boy presented with a speech delay. Retrospective analysis of his psychomotor development indicated that he had spoken his first words at around age 12 months. At age 3 years, he exhibited an articulation deficit, poor vocabulary, and syntactic difficulties. He was treated with intensive speech therapy for 6 months at age 5 years, without any improvement. At age 6 years, neurologic and general clinical examinations produced normal results, except for a slightly bulging skull on the left temporal side. His head circumference was at the 90th percentile. Language investigations revealed significant anomalies involving
N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47
45
Table 1. Neuropsychologic evolution of patient 1: Psychometric testing Timing (Day 0 Refers to Date of Shunting)
Presurgery
Month 12
Month 12
Month 28
Age
6y
7y
7y
8 y, 4 m
Month 48 10 y
Verbal IQ Performance IQ Full-scale IQ
WPPSI-R 105 82 93
WPPSI-R 117 98 109
WISC III 113 110 113
WISC III 116 108 107
WISC III 119 108 112
Language Assessment Timing (Day 0 Refers to Date of Shunting)
Presurgery
Month 6
Month 12
Month 28
Month 48
Age
6y
6 y, 6 m
7y
8 y, 4 m
10 y
Month 70 11 y, 10 m
Orofacial praxis Articulation Phonology, simple words Phonology, complex words Fluency Vocabulary, definition Vocabulary, designation Syntactic expression Syntactic comprehension
1.2 S.D. 1.6 S.D. 4 S.D. ND ND M M 1 S.D. M
1.2 S.D. 0.7 S.D. 3 S.D. ND ND 0.2 S.D. 0.6 S.D. 1 S.D. þ1.3 S.D.
1.2 S.D. 0.1 S.D. 0.7 S.D. 2 S.D. ND 0.2 S.D. þ0.3 S.D. M þ1 S.D.
þ0.1 S.D. M þ0.4 S.D. 2.2 S.D. þ0.6 S.D. ND ND ND ND
þ0.6 S.D. þ0.1 S.D. þ0.9 S.D. þ0.8 S.D. 0.3 S.D. þ1 S.D. þ0.6 S.D. M þ1 S.D.
þ0.6 þ0.1 þ0.9 0.5 0.6 ND ND ND ND
S.D. S.D. S.D. S.D. S.D.
Other Cognitive Assessments Timing (Day 0 Refers to Date of Shunting)
Month 6
Month 12
Month 28
Month 48
Month 70
Age
6 y, 6 m
7y
8 y, 4 m
10 y
11 y, 10 m
Verbal sequential memory Narrative memory Names memory Visual memory Constructive memory Inhibition Visual vigilance, speed Visual vigilance, accuracy Visual selective attention, speed Visual selective attention, accuracy Visual complex selective attention, speed Visual complex selective attention, accuracy Names reading Text reading, speed Text reading, accuracy Orthographic score
0.6 S.D. M M M 1 ND ND ND 3 S.D. 3 S.D. ND ND ND ND ND ND
1.3 S.D. ND þ1.5 S.D. ND M ND ND ND 3 S.D. 3 S.D. ND ND 0.2 S.D. ND ND 1.5 S.D.
1.6 S.D. 0.6 S.D. þ0.3 S.D. ND ND M 0.3 S.D. 3 S.D. þ3.5 S.D. þ1 S.D. þ0.5 S.D. 1 S.D. 1 S.D. M 0.6 S.D. 1 S.D.
ND ND M 2 S.D. ND ND 0.6 S.D. M þ0.5 S.D. þ1.5 S.D. 1.5 S.D. M M ND M 1 S.D.
ND ND ND ND ND 1.3 S.D. 1.6 S.D. 1 S.D. ND ND þ1 S.D. þ1 S.D. ND ND ND ND
Abbreviations: IQ ¼ Intelligence quotient m ¼ Month M ¼ Mean ND ¼ Not done S.D. ¼ Standard deviation WISC III ¼ Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition WPPSI-R ¼ Échelle d’Intelligence de Wechsler pour la Période Préscolaire et Primaire, Forme Révisée y ¼ Year articulation and phonology, and some limitations in syntax (Table 1). Verbal comprehension, lexical and syntactic expression, and full-scale intelligence quotient were normal. A full language assessment is provided in Table 1. When the patient was 6 years of age, cranial magnetic resonance imaging revealed a left temporal arachnoid cyst, causing a mass effect on the temporal lobe (Fig 1). A 24-hour electroencephalogram produced normal results. Positron emission tomography indicated a temporal asymmetry, with a decrease in fluorodeoxyglucose uptake of the left superior temporal gyrus, left basifrontal gyri, and left thalamus (Fig 2). At age 6 years, a cysto-peritoneal shunt was placed. Postoperative magnetic resonance imaging, 2 months after surgery, demonstrated the disappearance of the cyst and a full re-expansion of the temporal parenchyma (Fig 1). Positron emission tomography at 21 months postoperatively revealed a symmetric temporal signal (Fig 2). His speech therapy was continued, using the same methods as before surgery. His phonology improved first, and reached a normal level at 12 months postoperatively. Neuropsychologic assessments, repeated from 6-70 months postoperatively, revealed rapid and significant language improvement, as well as significant progress in his intelligence quotient. His full-scale intelligence quotient increased from 93 to 112 (Table 1). Several aspects of attention also improved significantly. No learning or behavioral difficulties were evident at school. Patient 2 This 7-year-old, right-handed boy was admitted for chronic headaches of increasing intensity. Since age 6 years, he had complained of recurrent acute headaches, occurring in the morning or during the night, accompanied by occasional
vomiting. He had no previous contributing medical history, and his early psychomotor development was uneventful. His school performance was good. General and neurologic clinical examinations produced normal results. Systematic neuropsychologic investigations (Table 2) revealed deficits in verbal comprehension (speech comprehension, 3 S.D.; syntactic comprehension, 1.7 S.D.) and metalinguistic function (definition of words, 1.7 S.D.). Other linguistic functions, such as oral praxis, articulation, phonology, verbal fluency, phonology, and syntactic verbal expression were normal or borderline. An assessment of his selective attention indicated deficits, i.e., 0.5 S.D. in speed, and 2 S.D. in precision. His full-scale intelligence quotient was normal. Cranial magnetic resonance imaging, performed at age 8 years, displayed a voluminous arachnoid cyst, located at the base of the left sylvian fissure, causing a mass effect on the anterior part of the left temporal lobe (data not shown). A 24-hour electroencephalogram demonstrated rare and very short bursts of generalized spike-wave activity during rapid eye movement sleep and waking. A cysto-peritoneal shunt was placed. His headaches disappeared a few days after the operation. Magnetic resonance imaging at 5 months after surgery indicated a decrease in cyst volume (data not shown). A 24-hour electroencephalogram was performed 9 months after surgery, and produced results similar to those of the preoperative recording. During 6 months, neuropsychologic follow-up indicated rapid and dramatic recovery (Table 2). A neuropsychologic assessment at 6 months after surgery indicated a significant improvement in verbal comprehension. His speech comprehension improved from 3 S.D. to þ1 S.D. His comprehension of complex instructions increased from 1.7 S.D. to þ1.7 S.D. Vocabulary definitions improved significantly, from 1.7 S.D. to 0.3 S.D. Selective attention significantly increased from 0.5 S.D. to þ1.5 S.D. in speed, and from 2 S.D. to 0.5 S.D. in precision. His intelligence
46
N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47
Figure 1. Cranial magnetic resonance image of patient 1, before (a) and after (b) shunting. On preoperative magnetic resonance imaging (spin-echo sequences, T2-weighted axial planes), the irregular inner wall of the left temporal arachnoid cyst is clearly delineated, without evidence of associated dysplasia. The postoperative study, carried out 2 months after cysto-peritoneal shunting, reveals a re-expansion of cortical tissue. quotient values remained stable, with a verbal intelligence quotient of 98 and a performance intelligence quotient of 105.
Discussion We report on two pediatric patients with left temporal arachnoid cysts and impaired language development, who exhibited rapid and significant improvement after late cysto-peritoneal shunting. Various data support the cause-and-effect relationship between this surgical treatment and cognitive improvement: (1) the close temporal relationship between statistically significant improvements in linguistic symptoms and surgical treatment; (2) documentation by positron emission tomography of significantly increased metabolic activity in the affected temporal lobe after
surgery; and (3) a correlation between the profile of language impairments and the location of mass effect. Patient 1 presented with hypometabolism of the left temporal superior gyrus, in the left basifrontal area, in concordance with his praxis, articulation, and phonologic impairments. Such an anatomic/functional relationship between the left temporal superior gyrus, basifrontal gyri, and phonologic treatment was previously documented in functional cerebral imaging studies [18]. Patient 1 presented with left thalamic hypometabolism. Implication of the left thalamus in articulation and phonologic functions was documented via anatomic/clinical correlations, e.g., in children presenting with a focal ischemic stroke [19], and also in a pediatric case of language impairment associated with a left temporal arachnoid cyst [7]. In that second case, the authors postulated that
Figure 2. Positron emission tomography images of patient 1, before (a) and after (b) shunting. The resting [18F] fludeoxyglucose uptake cranial images are spatially coregistered. Preoperative axial, coronal, and sagittal sections demonstrate prominent hypometabolism in cortical regions surrounding the cyst, including the left superior temporal gyrus, left basifrontal area, and left thalamus. On the postoperative positron emission tomography scan, performed 21 months after drainage, a marked improvement of glucose utilization is evident in all brain areas. The superior temporal gyrus and the thalamus regained normal, symmetric metabolism. The [18F] fludeoxyglucose incorporation (as an index for metabolic activity) is coded according to the color scale, expressed in percentages of maximal activity in the cortex. For a better comparison of the regional pattern, each study was rescaled to its own maximum. The cursor lines indicate a voxel in the left insula near to the lateral sulcus (x, y, and z (mm) ¼ 38, 18, and 2; coordinates with reference to the Talairach system). L, left side of the brain.
N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47 Table 2. Neuropsychologic evolution of patient 2: Psychometric testing Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7 y, 3 m
8 y, 11 m
WISC III Verbal IQ Performance IQ Full-scale IQ
97 107 102
98 105 102
Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7 y, 3 m
8 y, 11 m
Definition Complex instructions Syntactic comprehension Syntactic expression Orofacial praxis Articulation Phonology, simple words Phonology, complex words Verbal fluency Denomination words Designation words
1.7 S.D. 1.7 S.D. 3 S.D. M þ0.6 S.D. þ1 S.D. þ2 S.D. þ1.2 S.D. 0.7 S.D. þ0.5 S.D. 1 S.D.
0.3 S.D. þ1.7 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1.5 S.D. þ0.3 S.D. ND 0.3 S.D.
Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7, y 3 m
8 y, 11 m
Verbal sequential memory Motor sequential memory Sentences memory Narrative memory Words memory Visual memory Constructive memory Visual selective attention, speed Visual attention, accuracy
þ0.3 S.D. 0.7 S.D. ND 0.3 S.D. þ2 S.D. ND ND 0.5 S.D. 2 S.D.
þ0.3 S.D. 0.7 S.D. þ0.4 S.D. 0.3 S.D. þ2 S.D. 0.3 S.D. 0.5 S.D. þ1.5 S.D. 0.5 S.D.
Language Assessment
Other Cognitive Assessments
Abbreviations: IQ ¼ Intelligence quotient m ¼ Month M ¼ Mean ND ¼ Not done S.D. ¼ Standard deviation WISC III ¼ Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition y ¼ Year
such remote thalamic hypometabolism may be attributable to a deafferentation of thalamo-temporal projections [7]. Patient 2 presented with left temporal inferior compression, in concordance with his difficulties in linguistic comprehension. Indeed, classic neuropsychologic observations, and more recent functional cerebral imagery studies, indicate a correlation between comprehension capacities and the left anterior and inferior temporal gyri [20]. To our knowledge, language dysfunctions in the absence of symptomatic epilepsia were only reported in association with arachnoid cysts in a few pediatric patients [6-13]. These reports indicate impairment in linguistic functions, including anomalies in expressive language, verbal learning/memory, and the delayed and spontaneous recall of words. Intelligence quotients were often affected, in combination with memory deficits, learning problems, and psychomotor speed and attention difficulties, as observed in our patients [6-13]. A significant improvement in intelligence quotient was detected after surgery in six of 11 tested children from the literature, including those of the present study [6,7,9,13]. One of the only children in the literature who underwent postsurgical detailed language and functional imaging assessments presented with a normalization of speech abilities, associated with a reexpansion of the brain parenchyma, and an increase in brain metabolism adjacent to the cyst [7]. This report, in conjunction
47
with ours, supports (as stated by Wester [9]) the idea that large arachnoid cysts can alter cognitive function, but in a reversible manner, thus allowing for functional recovery after surgical treatment, even if such surgery is performed well after the onset of signs. Neither the literature nor our experience can clarify why some patients respond to surgical treatment, and others apparently do not. Unfortunately, the rarity of reports, the limitations of clinical or neuroradiologic data, and sometimes the brief duration of follow-up make it difficult to extract any clear predictive factors of therapeutic response from the present cases. This point would be worth addressing in future studies. In conclusion, our observations reinforce the rationale for neuroradiologic and thorough neuropsychologic assessments of patients with either specific cognitive impairments or arachnoid cysts, or both, and encourage clinicians to weigh the risk vs efficacy of surgical treatment for arachnoid cysts associated with neurologic impairment, even at a relatively advanced developmental age. We thank Marie-Cécile Nassogne, MD, PhD for her support. We are grateful to Isabelle Rapin, MD for helpful discussion. This work was supported by a Canadian Institute of Health Research grant (G.S.), a Fonds de Recherche en Santé du Québec scholarship (G.S.), and grants from La Fondation des Etoiles (G.S.) and Le Centre de Neurosciences de l’Université de Sherbrooke (G.S.). G.S. is a member of the Fonds de Recherche en Santé du Québec-funded Centre de Recherche Clinique Étienne-Le Bel.
References [1] Catala M, Poirier J. Arachnoid cysts: Histologic, embryologic and physiopathologic review. Rev Neurol 1998;154:489e501. [2] Wester K, Moen G. Documented growth of a temporal arachnoid cyst. J Neurol Neurosurg Psychiatry 2000;69:699e700. [3] Okumura Y, Sakaki T, Hirabayashi H. Middle cranial fossa arachnoid cyst developing in infancy: Case report. J Neurosurg 1995;82:1075e7. [4] Yamauchi T, Saeki N, Yamaura A. Spontaneous disappearance of temporofrontal arachnoid cyst in a child. Acta Neurochir (Wien) 1999;141:537e40. [5] Stowe LA, Go KG, Pruim J, den Dunnen W, Meiners LC, Paans AM. Language localization in cases of left temporal lobe arachnoid cyst: Evidence against interhemispheric reorganization. Brain Lang 2000;75:347e58. [6] Soukup VM, Patterson J, Trier TT, Chen JW. Cognitive improvement despite minimal arachnoid cyst decompression. Brain Dev 1998;20:589e93. [7] De Volder AG, Michel C, Thauvoy C, Willems G, Ferrière G. Brain glucose utilisation in acquired childhood aphasia associated with a sylvian arachnoid cyst: Recovery after shunting as demonstrated by PET. J Neurol Neurosurg Psychiatry 1994;57:296e300. [8] Wang PJ, Lin HC, Liu HM, Tseng CL, Shen YZ. Intracranial arachnoid cysts in children: Related signs and associated anomalies. Pediatr Neurol 1998;19: 100e4. [9] Wester K. Intracranial arachnoid cysts: Do they impair mental functions? J Neurol 2008;255:1113e20. [10] Wester K, Hugdahl K. Arachnoid cysts of the left temporal fossa: Impaired preoperative cognition and postoperative improvement. J Neurol Neurosurg Psychiatry 1995;59:293e8. [11] Wester K, Hugdahl K. Verbal laterality and handedness in patients with intracranial arachnoid cysts. J Neurol 2003;250:36e41. [12] Zaatreh MM, Bates ER, Hooper SR, et al. Morphometric and neuropsychologic studies in children with arachnoid cysts. Pediatr Neurol 2002;26:134e8. [13] Pierre-Kahn A, Capelle L, Brauner R, et al. Presentation and management of suprasellar arachnoid cysts: Review of 20 cases. J Neurosurg 1990;73:355e9. [14] Fewel ME, Levy ML, McComb JG. Surgical treatment of 95 children with 102 intracranial arachnoid cysts. Pediatr Neurosurg 1996;25:165e73. [15] Sommer IE, Smit LM. Congenital supratentorial arachnoidal and giant cysts in children: A clinical study with arguments for a conservative approach. Childs Nerv Syst 1997;13:8e12. [16] Pascual-Castroviejo I, Roche MC, Martinez Bermejo A, Arcas J, Garcia Blazquez M. Primary intracranial arachnoidal cysts: A study of 67 childhood cases. Childs Nerv Syst 1991;7:257e63. [17] Oberbauer RW, Haase J, Pucher R. Arachnoid cysts in children: A European cooperative study. Childs Nerv Syst 1992;8:281e6. [18] Démonet JF, Chollet F, Ramsay S, et al. The anatomy of phonological and semantic processing in normal subjects. Brain 1992;115:1753e68. [19] Gout A, Seibel N, Rouvière C, et al. Aphasia owing to subcortical brain infarcts in childhood. J Child Neurol 2005;20:1003e8. [20] Papathanassiou D, Etard O, Mellet E, Zago L, Mazoyer B, Tzourio-Mazoyer N. A common language network for comprehension and production: A contribution to the definition of language epicentres with PET. Neuroimage 2000;11:347e57.
Contents lists available at ScienceDirect
Pediatric Neurology journal homepage: www.elsevier.com/locate/pnu
Case Report
Language Impairment Associated With Arachnoid Cysts: Recovery After Surgical Treatment Nicole Laporte BSc a, Anne De Volder MD, PhD a, Christine Bonnier MD, PhD a, Christian Raftopoulos MD, PhD b, Guillaume Sébire MD, PhD c, * a
Service de Neuropédiatrie, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Brussels, Belgium Service de Neurochirurgie, Cliniques Universitaires Saint Luc, Université Catholique de Louvain, Brussels, Belgium c Service de Neurologie Pédiatrique, Centre Hospitalier Universitaire de Sherbrooke, Faculté de Médecine, Université de Sherbrooke, Sherbrooke, Quebec, Canada b
article information
abstract
Article history: Received 23 May 2010 Accepted 3 October 2011
Supporting data from the literature, we observe that large arachnoid cysts may affect cognitive function. Neuropsychologic assessment plus magnetic resonance imaging allowed for documentation of associations between left temporal arachnoid cysts, language impairment, and other cognitive dysfunctions. Significant cognitive improvements were evident soon after cysto-peritoneal shunting. These observations reinforce the rationale for neuropsychologic assessments of patients with developmental delay and arachnoid cysts, and support the potential benefit of surgical decompression for arachnoid cysts associated with neurologic deficits, even if surgery is performed well after the occurrence of neurologic deficits. Ó 2012 Elsevier Inc. All rights reserved.
Introduction Most arachnoid cysts are congenital, likely arising by the anomalous splitting of the arachnoidal layer of the meninges [1-3]. They are usually discovered incidentally during neuroimaging of asymptomatic patients [1]. However, certain clinical manifestations related to arachnoid cysts were reported, such as headaches, enlargements of head circumference, temporal bulging, intracranial hypertension, and partial seizures [2-17]. Only a few studies have dealt with cognitive dysfunctions associated with arachnoid cysts in childhood [5-13]. We report on two patients with arachnoid cysts adjacent to the temporal pole. Both patients presented with developmental language impairment, and both patients exhibited a rapid and significant language improvement postoperatively. Patients and Methods We retrospectively studied two patients presenting with arachnoid cysts associated with cognitive impairment. Both children were admitted between 1997 and 2002 in the Department of Child Neurology and Department of Neurosurgery at the Cliniques Universitaires Saint-Luc (Université Catholique de Louvain, Brussels, Belgium). During this timeframe, no other patients with clinically symptomatic * Communications should be addressed to: Dr. Sébire; Service de Neurologie Pédiatrique; Centre Hospitalier Universitaire de Sherbrooke; Faculté de Médecine; Université de Sherbrooke; 3001 12ème Avenue Nord; Sherbrooke, Quebec J1H5N4, Canada. E-mail address: [email protected] 0887-8994/$ - see front matter Ó 2012 Elsevier Inc. All rights reserved. doi:10.1016/j.pediatrneurol.2011.10.001
arachnoid cysts were recruited. These two patients underwent serial clinical, neuroradiologic (1.5 T cranial magnetic resonance imaging in patients 1 and 2, and positron emission tomography, i.e., an [18F] fludeoxyglucose scan, in patient 1), and neuropsychologic and language assessments before and after neurosurgical treatment. We paid particular attention to cognitive outcomes, focusing on linguistic functions that were deficient before surgery. The durations of follow-up were 6 years for patient 1, and 18 months for patient 2. Psychometric investigations were performed using the Échelle d’Intelligence de Wechsler pour la Période Préscolaire et Primaire (or its revised form) and the Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition. Language assessment was performed using the Epreuves pour l’Examen du Language, the Batterie d’Evaluation Psycholinguistique, the Nouvelles Epreuves pour l’Examen du Language, the Batterie Language Oral-Language Ecrit-Attention, the Test de Vocabulaire Actif et Passif, the Evaluation des Aptitudes Syntaxiques, and the Epreuves de Compréhension Syntaxique Sémantique. Memory was measured with specific subtests of Korkman’s Developmental Neuropsychological Assessment, the Batterie pour l’Examen Psychologique de l’Enfant, the Figure de Rey, the Auditory Verbal Learning Test, and the Epreuves de Reconnaissance Verbale. Attention was measured according to the Test de Zazzo, i.e., the Test of Everyday Attention. School learning level was measured with the Tests Pédagogiques du Premier Cycle Primaire, the Epreuves d’Apprentissage Scolaire Primaire, the Lecture de Mots et Compréhension, and Le Poucet. Patient 1 This 6-year-old, right-handed boy presented with a speech delay. Retrospective analysis of his psychomotor development indicated that he had spoken his first words at around age 12 months. At age 3 years, he exhibited an articulation deficit, poor vocabulary, and syntactic difficulties. He was treated with intensive speech therapy for 6 months at age 5 years, without any improvement. At age 6 years, neurologic and general clinical examinations produced normal results, except for a slightly bulging skull on the left temporal side. His head circumference was at the 90th percentile. Language investigations revealed significant anomalies involving
N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47
45
Table 1. Neuropsychologic evolution of patient 1: Psychometric testing Timing (Day 0 Refers to Date of Shunting)
Presurgery
Month 12
Month 12
Month 28
Age
6y
7y
7y
8 y, 4 m
Month 48 10 y
Verbal IQ Performance IQ Full-scale IQ
WPPSI-R 105 82 93
WPPSI-R 117 98 109
WISC III 113 110 113
WISC III 116 108 107
WISC III 119 108 112
Language Assessment Timing (Day 0 Refers to Date of Shunting)
Presurgery
Month 6
Month 12
Month 28
Month 48
Age
6y
6 y, 6 m
7y
8 y, 4 m
10 y
Month 70 11 y, 10 m
Orofacial praxis Articulation Phonology, simple words Phonology, complex words Fluency Vocabulary, definition Vocabulary, designation Syntactic expression Syntactic comprehension
1.2 S.D. 1.6 S.D. 4 S.D. ND ND M M 1 S.D. M
1.2 S.D. 0.7 S.D. 3 S.D. ND ND 0.2 S.D. 0.6 S.D. 1 S.D. þ1.3 S.D.
1.2 S.D. 0.1 S.D. 0.7 S.D. 2 S.D. ND 0.2 S.D. þ0.3 S.D. M þ1 S.D.
þ0.1 S.D. M þ0.4 S.D. 2.2 S.D. þ0.6 S.D. ND ND ND ND
þ0.6 S.D. þ0.1 S.D. þ0.9 S.D. þ0.8 S.D. 0.3 S.D. þ1 S.D. þ0.6 S.D. M þ1 S.D.
þ0.6 þ0.1 þ0.9 0.5 0.6 ND ND ND ND
S.D. S.D. S.D. S.D. S.D.
Other Cognitive Assessments Timing (Day 0 Refers to Date of Shunting)
Month 6
Month 12
Month 28
Month 48
Month 70
Age
6 y, 6 m
7y
8 y, 4 m
10 y
11 y, 10 m
Verbal sequential memory Narrative memory Names memory Visual memory Constructive memory Inhibition Visual vigilance, speed Visual vigilance, accuracy Visual selective attention, speed Visual selective attention, accuracy Visual complex selective attention, speed Visual complex selective attention, accuracy Names reading Text reading, speed Text reading, accuracy Orthographic score
0.6 S.D. M M M 1 ND ND ND 3 S.D. 3 S.D. ND ND ND ND ND ND
1.3 S.D. ND þ1.5 S.D. ND M ND ND ND 3 S.D. 3 S.D. ND ND 0.2 S.D. ND ND 1.5 S.D.
1.6 S.D. 0.6 S.D. þ0.3 S.D. ND ND M 0.3 S.D. 3 S.D. þ3.5 S.D. þ1 S.D. þ0.5 S.D. 1 S.D. 1 S.D. M 0.6 S.D. 1 S.D.
ND ND M 2 S.D. ND ND 0.6 S.D. M þ0.5 S.D. þ1.5 S.D. 1.5 S.D. M M ND M 1 S.D.
ND ND ND ND ND 1.3 S.D. 1.6 S.D. 1 S.D. ND ND þ1 S.D. þ1 S.D. ND ND ND ND
Abbreviations: IQ ¼ Intelligence quotient m ¼ Month M ¼ Mean ND ¼ Not done S.D. ¼ Standard deviation WISC III ¼ Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition WPPSI-R ¼ Échelle d’Intelligence de Wechsler pour la Période Préscolaire et Primaire, Forme Révisée y ¼ Year articulation and phonology, and some limitations in syntax (Table 1). Verbal comprehension, lexical and syntactic expression, and full-scale intelligence quotient were normal. A full language assessment is provided in Table 1. When the patient was 6 years of age, cranial magnetic resonance imaging revealed a left temporal arachnoid cyst, causing a mass effect on the temporal lobe (Fig 1). A 24-hour electroencephalogram produced normal results. Positron emission tomography indicated a temporal asymmetry, with a decrease in fluorodeoxyglucose uptake of the left superior temporal gyrus, left basifrontal gyri, and left thalamus (Fig 2). At age 6 years, a cysto-peritoneal shunt was placed. Postoperative magnetic resonance imaging, 2 months after surgery, demonstrated the disappearance of the cyst and a full re-expansion of the temporal parenchyma (Fig 1). Positron emission tomography at 21 months postoperatively revealed a symmetric temporal signal (Fig 2). His speech therapy was continued, using the same methods as before surgery. His phonology improved first, and reached a normal level at 12 months postoperatively. Neuropsychologic assessments, repeated from 6-70 months postoperatively, revealed rapid and significant language improvement, as well as significant progress in his intelligence quotient. His full-scale intelligence quotient increased from 93 to 112 (Table 1). Several aspects of attention also improved significantly. No learning or behavioral difficulties were evident at school. Patient 2 This 7-year-old, right-handed boy was admitted for chronic headaches of increasing intensity. Since age 6 years, he had complained of recurrent acute headaches, occurring in the morning or during the night, accompanied by occasional
vomiting. He had no previous contributing medical history, and his early psychomotor development was uneventful. His school performance was good. General and neurologic clinical examinations produced normal results. Systematic neuropsychologic investigations (Table 2) revealed deficits in verbal comprehension (speech comprehension, 3 S.D.; syntactic comprehension, 1.7 S.D.) and metalinguistic function (definition of words, 1.7 S.D.). Other linguistic functions, such as oral praxis, articulation, phonology, verbal fluency, phonology, and syntactic verbal expression were normal or borderline. An assessment of his selective attention indicated deficits, i.e., 0.5 S.D. in speed, and 2 S.D. in precision. His full-scale intelligence quotient was normal. Cranial magnetic resonance imaging, performed at age 8 years, displayed a voluminous arachnoid cyst, located at the base of the left sylvian fissure, causing a mass effect on the anterior part of the left temporal lobe (data not shown). A 24-hour electroencephalogram demonstrated rare and very short bursts of generalized spike-wave activity during rapid eye movement sleep and waking. A cysto-peritoneal shunt was placed. His headaches disappeared a few days after the operation. Magnetic resonance imaging at 5 months after surgery indicated a decrease in cyst volume (data not shown). A 24-hour electroencephalogram was performed 9 months after surgery, and produced results similar to those of the preoperative recording. During 6 months, neuropsychologic follow-up indicated rapid and dramatic recovery (Table 2). A neuropsychologic assessment at 6 months after surgery indicated a significant improvement in verbal comprehension. His speech comprehension improved from 3 S.D. to þ1 S.D. His comprehension of complex instructions increased from 1.7 S.D. to þ1.7 S.D. Vocabulary definitions improved significantly, from 1.7 S.D. to 0.3 S.D. Selective attention significantly increased from 0.5 S.D. to þ1.5 S.D. in speed, and from 2 S.D. to 0.5 S.D. in precision. His intelligence
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N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47
Figure 1. Cranial magnetic resonance image of patient 1, before (a) and after (b) shunting. On preoperative magnetic resonance imaging (spin-echo sequences, T2-weighted axial planes), the irregular inner wall of the left temporal arachnoid cyst is clearly delineated, without evidence of associated dysplasia. The postoperative study, carried out 2 months after cysto-peritoneal shunting, reveals a re-expansion of cortical tissue. quotient values remained stable, with a verbal intelligence quotient of 98 and a performance intelligence quotient of 105.
Discussion We report on two pediatric patients with left temporal arachnoid cysts and impaired language development, who exhibited rapid and significant improvement after late cysto-peritoneal shunting. Various data support the cause-and-effect relationship between this surgical treatment and cognitive improvement: (1) the close temporal relationship between statistically significant improvements in linguistic symptoms and surgical treatment; (2) documentation by positron emission tomography of significantly increased metabolic activity in the affected temporal lobe after
surgery; and (3) a correlation between the profile of language impairments and the location of mass effect. Patient 1 presented with hypometabolism of the left temporal superior gyrus, in the left basifrontal area, in concordance with his praxis, articulation, and phonologic impairments. Such an anatomic/functional relationship between the left temporal superior gyrus, basifrontal gyri, and phonologic treatment was previously documented in functional cerebral imaging studies [18]. Patient 1 presented with left thalamic hypometabolism. Implication of the left thalamus in articulation and phonologic functions was documented via anatomic/clinical correlations, e.g., in children presenting with a focal ischemic stroke [19], and also in a pediatric case of language impairment associated with a left temporal arachnoid cyst [7]. In that second case, the authors postulated that
Figure 2. Positron emission tomography images of patient 1, before (a) and after (b) shunting. The resting [18F] fludeoxyglucose uptake cranial images are spatially coregistered. Preoperative axial, coronal, and sagittal sections demonstrate prominent hypometabolism in cortical regions surrounding the cyst, including the left superior temporal gyrus, left basifrontal area, and left thalamus. On the postoperative positron emission tomography scan, performed 21 months after drainage, a marked improvement of glucose utilization is evident in all brain areas. The superior temporal gyrus and the thalamus regained normal, symmetric metabolism. The [18F] fludeoxyglucose incorporation (as an index for metabolic activity) is coded according to the color scale, expressed in percentages of maximal activity in the cortex. For a better comparison of the regional pattern, each study was rescaled to its own maximum. The cursor lines indicate a voxel in the left insula near to the lateral sulcus (x, y, and z (mm) ¼ 38, 18, and 2; coordinates with reference to the Talairach system). L, left side of the brain.
N. Laporte et al. / Pediatric Neurology 46 (2012) 44e47 Table 2. Neuropsychologic evolution of patient 2: Psychometric testing Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7 y, 3 m
8 y, 11 m
WISC III Verbal IQ Performance IQ Full-scale IQ
97 107 102
98 105 102
Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7 y, 3 m
8 y, 11 m
Definition Complex instructions Syntactic comprehension Syntactic expression Orofacial praxis Articulation Phonology, simple words Phonology, complex words Verbal fluency Denomination words Designation words
1.7 S.D. 1.7 S.D. 3 S.D. M þ0.6 S.D. þ1 S.D. þ2 S.D. þ1.2 S.D. 0.7 S.D. þ0.5 S.D. 1 S.D.
0.3 S.D. þ1.7 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1 S.D. þ1.5 S.D. þ0.3 S.D. ND 0.3 S.D.
Timing (Day 0 Refers to Date of Shunting)
Before Surgery
Month 6 After Surgery
Age
7, y 3 m
8 y, 11 m
Verbal sequential memory Motor sequential memory Sentences memory Narrative memory Words memory Visual memory Constructive memory Visual selective attention, speed Visual attention, accuracy
þ0.3 S.D. 0.7 S.D. ND 0.3 S.D. þ2 S.D. ND ND 0.5 S.D. 2 S.D.
þ0.3 S.D. 0.7 S.D. þ0.4 S.D. 0.3 S.D. þ2 S.D. 0.3 S.D. 0.5 S.D. þ1.5 S.D. 0.5 S.D.
Language Assessment
Other Cognitive Assessments
Abbreviations: IQ ¼ Intelligence quotient m ¼ Month M ¼ Mean ND ¼ Not done S.D. ¼ Standard deviation WISC III ¼ Échelle d’Intelligence de Wechsler pour Enfants, Troisième Édition y ¼ Year
such remote thalamic hypometabolism may be attributable to a deafferentation of thalamo-temporal projections [7]. Patient 2 presented with left temporal inferior compression, in concordance with his difficulties in linguistic comprehension. Indeed, classic neuropsychologic observations, and more recent functional cerebral imagery studies, indicate a correlation between comprehension capacities and the left anterior and inferior temporal gyri [20]. To our knowledge, language dysfunctions in the absence of symptomatic epilepsia were only reported in association with arachnoid cysts in a few pediatric patients [6-13]. These reports indicate impairment in linguistic functions, including anomalies in expressive language, verbal learning/memory, and the delayed and spontaneous recall of words. Intelligence quotients were often affected, in combination with memory deficits, learning problems, and psychomotor speed and attention difficulties, as observed in our patients [6-13]. A significant improvement in intelligence quotient was detected after surgery in six of 11 tested children from the literature, including those of the present study [6,7,9,13]. One of the only children in the literature who underwent postsurgical detailed language and functional imaging assessments presented with a normalization of speech abilities, associated with a reexpansion of the brain parenchyma, and an increase in brain metabolism adjacent to the cyst [7]. This report, in conjunction
47
with ours, supports (as stated by Wester [9]) the idea that large arachnoid cysts can alter cognitive function, but in a reversible manner, thus allowing for functional recovery after surgical treatment, even if such surgery is performed well after the onset of signs. Neither the literature nor our experience can clarify why some patients respond to surgical treatment, and others apparently do not. Unfortunately, the rarity of reports, the limitations of clinical or neuroradiologic data, and sometimes the brief duration of follow-up make it difficult to extract any clear predictive factors of therapeutic response from the present cases. This point would be worth addressing in future studies. In conclusion, our observations reinforce the rationale for neuroradiologic and thorough neuropsychologic assessments of patients with either specific cognitive impairments or arachnoid cysts, or both, and encourage clinicians to weigh the risk vs efficacy of surgical treatment for arachnoid cysts associated with neurologic impairment, even at a relatively advanced developmental age. We thank Marie-Cécile Nassogne, MD, PhD for her support. We are grateful to Isabelle Rapin, MD for helpful discussion. This work was supported by a Canadian Institute of Health Research grant (G.S.), a Fonds de Recherche en Santé du Québec scholarship (G.S.), and grants from La Fondation des Etoiles (G.S.) and Le Centre de Neurosciences de l’Université de Sherbrooke (G.S.). G.S. is a member of the Fonds de Recherche en Santé du Québec-funded Centre de Recherche Clinique Étienne-Le Bel.
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