How Important Is to Know the Psychosocial Performance in an Operated Child of Meningioma? Devil Is in the Details.

BACKGROUND: Meningioma constitutes only 0.4%-4.1% of all the pediatric tumors. This article aims to find the impact of the pediatric meningioma surgery on the developmental and scholastic performance among these children over long-term follow-up.
MATERIALS AND METHODS: This study is a retrospective analysis of all the histopathological proven pediatric meningioma and a cross-sectional analysis to study the functional outcome, using Malin's Intelligence Scale for Indian children (MISIC); scholastic performance was assessed from behavioral checklist for screening the learning disabled (BCSLD) and subjective self-filled questionnaire to know parent satisfaction.
RESULTS: Twenty-eight patients (mean age 14.52 ± 0.722 years) (M:F = 16:12) were analyzed (6 [21.4%] were grade-schooler and 22 [78.5%] were teenage), with most common symptom being headache (n = 20, 71.4%) and mean duration of symptoms was 11.19 ± 16.25 days. The mean intelligent quotient (IQ) of grade-schooler was 83.4 ± 9.072 compared to 75.69 ± 9.903 among teenage group. The BCSLD analyses showed that the postoperative score was poorer. Similarly, an average change in BCSLD was observed among the patients with complications (10) compared to the patients without complication (8).
CONCLUSION: The discontinuation in schooling or lack of alternative education may lead to poor MISIC scores, wrongly categorizing the children in poor IQ group. In pediatric benign disease such as meningioma, the holistic approach should be opted from the time of first visit to neurological care team. Copyright:

INTRODUCTION

Pediatric meningioma is rarely encountered in clinical practice, but deserves utmost care, owing to good surgical outcome and long-term survival. Meningioma constitutes only 0.4%–4.1% of all the pediatric tumors.[1] Despite looking similar, at first glance, pediatric meningioma possesses certain important differences from adult variant, like clinical presentation and biological characteristics.[23] Nonetheless, the rarity of tumor, limits a focused, large sample–sized studies or any article with a long-term follow-up.[4] Apart from technical expertise, these pediatric patients demand a more attentive protocol and a multidisciplinary care. The pediatric meningioma is less aggressive than their adult counterpart, so these children retain a near-normal life after surgery. However, the neurosurgery may have a considerable impact on their physical and mental profile. Considering these children as the future of a country, it is our responsibility to highlight the undiscussed, but necessary facts, what we have experienced over last two decades. This article aimed to find the impact of the pediatric meningioma surgery on the developmental and scholastic performance of these children over long-term follow-up.

MATERIALS AND METHODS

Study design

Individual consent to use clinical and radiological details for publication was obtained from each patient as per our departmental protocol. Our study is a single-institutional observational study (1999–2019), wherein a retrospective analysis of prospectively maintained data was done. All the histopathological proven patients of meningioma with age less than 18 years were included. Further, a postoperative cross-sectional analysis of all the included patients was done (by a child psychiatrist and psychologist) to study the functional outcome, scholastic performance, and subjective parent satisfaction following the acceptable questionnaire scale.

Study parameters

The clinical parameters include demographic profile, symptoms and neurological findings, radiological findings (including location, extent, and pattern), histopathology, World Health Organization (WHO) grade 2016, extent of tumor excision, recurrence, and surgical outcome. The functional outcome was assessed using (1) Malin’s Intelligence Scale for Indian Children (MISIC), (2) scholastic performance was assessed from behavioral checklist for screening the learning disabled (BCSLD), and subjective self-filled questionnaire to know parent satisfaction. All the parents were asked “whether you are satisfied by developmental and mental growth of our child as compared to other children of his classroom” (response category includes “satisfied” or “not satisfied”). The above scorings were done by one child psychiatrist and child psychologist individually.

Subgroup analyses

All the included patients were further grouped as grade-schooler (5–12 years) and teenage (13–18 years), and study parameters were compared to know whether age is an independent causal factor.

Statistical analyses

We used Statistical Package for the Social Sciences (IBM, New York, version 20.0) software. A P value of less than 0.05 was considered as significant. Chi-square and Fischer’s exact test were used to compare the study parameters among the groups.

RESULTS

Clinical parameters

A total of 29 patients were called, but one patient (age 3 years) was excluded (he did not turn up for functional assessment). As such, 28 patients (mean age 14.52 ± 0.722 years) (M:F = 16:12) were finally analyzed. Among these, 6 (21.4%) were grade-schooler and 22 (78.5%) were teenage. The most common symptom was headache (n = 20, 71.4%), followed by seizure (n = 12, 42.8%), and vomiting and visual deficits (n = 10, 35.7%). The mean duration of symptoms was 11.19 ± 16.25 days. Table 1 summarizes different location of tumors in our study, and the most common location was middle skull base (n = 8, 28.5%). A Simpson’s grade I excision was possible in all patients of convexity and parasagittal meningioma [Figures 1 and 2]. Grade II excision could be possible in anterior skull base meningioma. However, in the middle skull base tumors, grade IV excision was done, due to its close anatomical relation with important vasculature and cranial nerves [Table 2]. The average size of tumor was 4 × 5 cm. Most of the meningiomas were firm in consistency (85.7%) and of moderate vascularity (n = 16, 57.1%). In three patients of middle skull base meningioma, internal carotid artery was encased, and the brain invasion was found in 13 patients. The most common histological type was meningothelial meningioma (28.6%) followed by transitional (25%). Table 1 summarizes surgical complications among the included patients. Of 10 cases who presented with visual deficit, six cases persisted with significant visual deficit. Of 12 cases who presented with seizure, two cases had persistent seizure, who required more than three antiepileptics to control the seizure even though patients had no complete control. Excluding one patient, who died on the same day of surgery, the mean duration of postoperative hospital stay was 12.07 ± 6.874 days.

Table 1

Clinical profile of all the patients included in our series

Clinical parameter	Number of patients	Percentage
Mean age (years)	14.52 ± 0.722
Gender (M:F)	16:12
Symptoms
Headache	20	71.42
Seizures	12	42.85
Vomiting	10	35.71
Motor deficit	5	17.85
Visual deficit	10	35.71
Cranial nerve palsies	2	6.89
Location
Anterior skull base	5	17.9
Middle skull base	8	28.6
Convexity	5	17.9
Falcine–parasagittal	6	21.4
Intraventricular	4	14.3
Surgical complication
Wound complication	3	10.71
Hematoma	1	3.57
Motor deficit	2	7.14
Cranial nerve palsies	2	7.14

Figure 1

Representative axial CT and MRI of a pediatric convexity meningioma patients. Child was operated 8 years back and doing well neurologically

Figure 2

Representative axial CT showing a case of convexity meningioma operated 16 years back, and axial MRI of a pediatric intraventricular meningioma, who was operated 11 years back. Both the children are doing well neurologically

Table 2

Simpson grade of excision according to the location

Location	Simpson’s grade of excision
	Grade I	Grade II	Grade IV
Convexity	5	0	1	6
Parasagittal	0	2	0	2
Falcine	0	2	1	3
Intraventricular	1	1	2	4
Anterior skull base	0	3	2	5
Middle skull base	1	2	5	8
Total	7	10	11	28

Functional outcome

Among all the patients, MISIC (Indian adaptation of Wechsler’s scoring) could be assessed in 18 patients. The mean intelligent quotient (IQ) of grade-schooler was 83.4 ± 9.072 compared to 75.69 ± 9.903 among teenage group [Table 3]. We found that the patients with low score fall in the category of low average to borderline category. The BCSLD analyses showed that the postoperative score was poorer [Table 4]. Further, when the scores were compared in patients with or without complications, average MISIC was lower among patients without complications (76 compared to 80). Similarly, an average change in BCSLD among the patients with complications was 10 compared to the patients without complication, being 8. Overall acceptance of our surgical outcome was good as 23 (82.14%) patients were satisfied. The mean duration of follow-up was 8.2 ± 2.1 (range, 4–21) years.

Table 3

Comparison of Malin’s intelligence scale for children included in our series

	Grade-schooler	Teenage
Mean	83.4 ± 9.072	75.69 ± 9.903
Median	85	77
Minimum/maximum	74/93	58/92
Interquartile range	18	16

Table 4

A bar graph showing postoperative change in scores of BCSLD as compared to preoperative period

Blue box = preoperative score, orange box = postoperative scores

DISCUSSION

Burden of pediatric meningioma

Pediatric meningioma constitutes 0.4%–4.1% of all the pediatric age tumors.[1] Contrary to male preponderance in adults, this subset of tumor is common in female children.[567] However, we found somewhat different results with male-dominating population (1.3:1). This difference may occur out of referral bias or a possible selection bias. The higher preponderance in adult female population is because of the influence of estrogen and progesterone, whereas this effect is masked in the pediatric population in children.[89] The mean age of patients in our study was 14.52 ± 0.722 years, which is similar to figures reported in other studies, ranging from 11 to 14 years.[1011] Headache, vomiting, and visual deficits are common symptoms in our study and also in other reported series.[101112] One interesting fact that need a mention here, is the delayed presentation of patients, because the symptoms of raised intracranial pressure are ignored, considering them as school tantrums.[13] Another similar symptom ignored is frequent change in the “diopter number” of glasses. The school teachers and parents must have a low threshold and consult a physician early, to mitigate harmful consequences. The most important factor governing the surgical outcome is the extent of tumor excision, which merely depends on the location and anatomical structures in vicinity of tumor. Because of the rarity of these tumors, the most common location is quoted differently in various published series.[1014,15] In our series, the most common tumor location was middle skull base, wherein grade IV excision was achieved. Grade I excision was achieved in all the cases of convexity and parasagittal meningioma. The adjuvant radiotherapy in grade I excised tumor was avoided, considering the long-term adverse side effects such as secondary tumor induction, hormonal deficiency, and growth and intellectual retardation.[12] We have closely followed these cases with clinical and radiological workup and preferred re-surgery over adjuvant radiotherapy.

How the pediatric meningioma is different?

These tumors tend to behave more aggressively in pediatric population [Figure 3]. Grade II and grade III is more common in pediatric groups.[1617] In our series, 35.7% were grade II and grade III meningioma, and two patients had recurrence. Greater mitotic rate, high proliferation indices, more brain invasion, and higher recurrence rates have been reported in pediatric meningioma.[318] A favorable fact is that despite its aggressiveness, tumor has better surgical outcome.[19] This favorable surgical outcome can also be attributed to location and less vascularity. One more indirect factor could be good brain plasticity in pediatric population.

Figure 3

Intraoperative photograph showing excised tumor in a child, wherein Simpson’s grade I excision was done

Behavioral and scholastic outcome after neurosurgery—What is the best age to intervene?

A good surgical resection is the key in the management of pediatric tumors. In a very young child (i.e., age less than 3 years), radiotherapy is avoided to prevent a long-term impact on growing brain. However, the residual tumor or a tumor in the eloquent region, may require fractionated radiotherapy. If recurrence occurs then re-surgery should be offered as first line of treatment.[20] We believe that the adequate “age to intervene” depends on the “facilities” and specialization level of institute. If one has a high end “pediatric” intensivist with good surgical expertise, age is no bar. Our result showed that age at surgery was not determining the functional outcome. We gave phenytoin sodium in all our cases as first-line antiepileptic drug.

Few series have highlighted the functional outcome of pediatric meningioma patients. In our study, a subjective functional outcome was assessed using a simple questionnaire by asking about parent’s view on development of their child after surgery. Of the patients, 23 of 27 (one died in perioperative period) were satisfied after surgery. Eighteen patients responded in the objective assessment, wherein subgroup analyses were also done. In the Indian teaching method, these subgroups have different methods of teaching. Also the grade-schooler children are more susceptible to adapt new pattern of learning as compared to teenage group. These 18 patients were assessed by our child psychologist by using MISIC, which is an Indian adaptation of internationally acceptable Wechsler’s scoring.[21] This scale assesses a child’s intelligence. The mean IQ of grade-schooler was 83.4 ± 9.072, whereas it was 75.69 ± 9.903 among the teenage group. To our surprise, all the patients had below average score, which is an alarming issue. As the sample size was small, we could not get statistical significance. The BCSLD, another tool to measure scholastic performance of children, was also used.[22] BCSLD consists of 30 positive or negative points, and we found that there was a significant change in scores of all patients as these patients lagged behind in their schooling. Maximum score was lost in cognition, memory and motor coordination.

So early diagnosis and maximum resection in the initial surgery, with minimum new-onset deficit should be the goal of surgery. With advent and utilization of new gadgets in operation room (OR), maximum-safe excision should be attempted, which will be translated in the early resumption of day-to-day activities, including the early resumption of schooling and/or alternate method of learning [Figure 4]. Thus a good surgical outcome is obviously influencing the good behavioral and mental outcome. Pogany et al.,[23] in his study of 2152 long-term survivors and 2432 controls (aged 5 to 37 years), found that the patients who survived had resulted in deficits in dexterity, ambulation, hearing, speech, and cognition. There were impairments in multiple domains but the impairment in cognition was most common, and that too was more frequent in the group of patients who were exposed to radiotherapy at younger age. Similarly, Barrera et al.,[24] in his study of 800 survivors (aged 17 years or younger), found that patients had poorer grades in school, learning disabilities, and had no close friends.

Figure 4

Representative clinical photograph showing swelling over vertex of the child and corresponding MRI showing convexity of meningioma

We also compared these parameters among patients, subgrouping them as “with or without complications” (wound complications, motor or cranial nerves deficit). In patients with complications, average MISIC score was 76, whereas in patients without complications, it was 80. Average change in BCSLD in patients with complications was ten, whereas in other group, it was eight. Although the result was not statistically significant, a clinical trend showing poorer functional outcome in the group of patient with “surgical technical complication” was seen.

We did not compare tumor size in our study (average tumor size was 4 × 5 cm), however, in previous studies, it has been shown that “tumor size” at diagnosis has no correlation at all with cognition at the time of diagnosis.[25] Contrarily, Tonning et al.[26] showed that pediatric brain tumor has inverse relationship with intelligent question. Tumor size is better predictor for cognitive sequelae than sex.

Limitation of the study

There may be several contributing factors to these low performances such as prolonged use of antiepileptic, motor deficits, and postoperative adjuvant radiotherapy. The persistent seizure and visual deficit were important factors delaying the reschooling and discontinuation in schooling. The socioeconomic status of family and extent of involvement of the caregivers are other important confounding factors. A prospective study with randomized population may provide more substantial results. The study can be extended, including other common benign tumorlike pilocytic astrocytoma and so on.

Future perspective

We propose that a psychologist should be involved, even before admission, and periodic follow-up must be scheduled. Parental involvement should be encouraged and the operating pediatric neurosurgeon plays a central role in coordinating the multidisciplinary team.

CONCLUSION

The delay in schooling or low IQ of these children will cost them significantly in future. The interruption or discontinuation in schooling as well as no alternative continuation of study, lead to poor MISIC scoring and wrongly labeling the children in poor IQ group. It is an addressable and a significant concern. In pediatric benign disease such as meningioma, the holistic approach should be opted from the time of first visit to neurological care team. Cure from seizure and minimal deficit with maximum safe and gross resection using all available latest tools should be the goal. The policy makers in developing country such as India should address this important issue.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent forms. In the form the patient(s) has/have given his/her/their consent for his/her/their images and other clinical information to be reported in the journal. The patients understand that their names and initials will not be published and due efforts will be made to conceal their identity, but anonymity cannot be guaranteed.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.