Endoscopic endonasal transsphenoidal approach for pediatric craniopharyngiomas: A case series

Journal Pre-proof Endoscopic endonasal transsphenoidal approach for pediatric craniopharyngiomas: a case series Juliana Carolina Schelini, Sergio Cavalheiro, Patrícia Alessandra Dastoli, Élcio Roldan Hirai, Camila Atallah, Marcos Costa, Jardel Nicacio, Andrea Maria Capellano, Nasjla Silva, Samuel Zymberg, Rodrigo de Paula Santos PII:

S0165-5876(19)30539-7

DOI:

https://doi.org/10.1016/j.ijporl.2019.109786

Reference:

PEDOT 109786

To appear in:

International Journal of Pediatric Otorhinolaryngology

Received Date: 3 October 2019 Revised Date:

14 November 2019

Accepted Date: 14 November 2019

Please cite this article as: J.C. Schelini, S. Cavalheiro, P.A. Dastoli, É.R. Hirai, C. Atallah, M. Costa, J. Nicacio, A.M. Capellano, N. Silva, S. Zymberg, R. de Paula Santos, Endoscopic endonasal transsphenoidal approach for pediatric craniopharyngiomas: a case series, International Journal of Pediatric Otorhinolaryngology, https://doi.org/10.1016/j.ijporl.2019.109786. This is a PDF file of an article that has undergone enhancements after acceptance, such as the addition of a cover page and metadata, and formatting for readability, but it is not yet the definitive version of record. This version will undergo additional copyediting, typesetting and review before it is published in its final form, but we are providing this version to give early visibility of the article. Please note that, during the production process, errors may be discovered which could affect the content, and all legal disclaimers that apply to the journal pertain. © 2019 Elsevier B.V. All rights reserved.

Title:

Endoscopic

endonasal

transsphenoidal

approach

for

pediatric

craniopharyngiomas: a case series

Authors: Juliana Carolina Schelini, M.D.1 Sergio Cavalheiro, M.D, PhD.2,3 Patrícia Alessandra Dastoli, M.D, PhD.2,3 Élcio Roldan Hirai, M.D.1 Camila Atallah, M.D.1 Marcos Costa, M.D, PhD.3 Jardel Nicacio, M.D, PhD.3 Andrea Maria Capellano, M.D, PhD.3 Nasjla Silva, M.D, PhD.3 Samuel Zymberg, M.D, PhD.2 Rodrigo de Paula Santos, M.D, PhD.1

1. Department of Otorhinolaryngology and Head and Neck Surgery, Federal University of São Paulo - UNIFESP 2. Discipline of Neurology and Neurosurgery, Federal University of São Paulo UNIFESP 3. Institute of Pediatric Oncology - IOP / GRAACC / UNIFESP 4. Departamento de Otorrinolaringologia e Cirurgia de Cabeça e Pescoço, Federal University of São Paulo - UNIFESP 5. Disciplina de Neurologia e Neurocirurgia, Federal University of São Paulo - UNIFESP 6. Instituto de Oncologia Pediátrica - IOP / GRAACC / UNIFESP

Corresponding author: Juliana Carolina Schelini Federal University of São Paulo – UNIFESP Rua Pedro de Toledo 943, Vila Clementino - CEP: 04039- 901 São Paulo, SP, Brazil e-mail: [email protected]

Conflicts of interests: None to declare

Financial disclosures: None to declare

Submission declaration: This manuscript has been submitted to this journal solely.

ABSTRACT Objectives: This study aims to analyze our series of pediatric patients who underwent craniopharyngioma resection using the endoscopic endonasal transsphenoidal approach (EETA). Methods: We collected clinical and surgical data from the charts of 20 children who underwent craniopharyngioma removal surgery using the EETA from 2007 to 2017. From the charts, we collected demographic information, results of imaging tests (size and extension of the tumor), and information regarding the surgical procedure and postoperative complications. Results: From the 20 patients included in this series (12 women and eight men), 17 underwent EETA as a primary procedure, and the remaining three underwent EETA as a secondary procedure due to a relapsing tumor following previous transcranial surgery. The mean age of the patients at the time of the surgical procedure was 7.5 years (range 3–18 years). Regarding their location, 12 tumors were in the sellar and suprasellar regions, three extended into the third ventricle, and five were exclusively intrasellar. We achieved a gross total resection (GTR) of the tumor in 14 patients (70%), subtotal in five (25%), and partial in one (5%). One patient (5%) developed a cerebrospinal fluid fistula after the surgical procedure. In the postoperative follow-up period (mean time=5.3 years; range=2-9 years), 11 (55%) patients developed panhypopituitarism, and a relapsing tumor was later found in three (15%) patients. Regarding visual impairment, four patients had visual abnormalities preoperatively (amaurosis, n=2; bilateral visual acuity decrease, n=1; bilateral visual field defect, n=1), and those did not improve or worsened postoperatively. None of the patients who did not have vision problems before the surgery developed those postoperatively. Conclusion: Our results showed that the EETA is a safe and effective approach for removing craniopharyngiomas in children, as it associated with low operative morbidity and complication rates. Also, our data demonstrated that the EETA may be performed regardless of the size of the nasal cavity, pneumatization of the sphenoid sinuses, and location or extension of the tumors.

Keywords: Craniopharyngioma; transsphenoidal approach; children

1.

INTRODUCTION

Craniopharyngiomas are rare benign tumors that typically arise from the remnants of the Rathke’s pouch, which is a cystic diverticulum that originates from the roof of the stomodeum. They comprise 3% to 5% of all primary brain tumors, accounting for 6% of all intracranial tumors in the pediatric population [1-4]. Also, they are the most common sellar and parasellar tumors in the pediatric population. [4] Epidemiologic data showed that there is no sex predilection. Regarding age, there is a bimodal age distribution within the first and second decades of life (5-14 years) and after the 5th decade (50-74 years). There are two histological subtypes: (1) adamantinous, which is more frequent in the first two decades of life but may occur in people of all ages; and (2) papillary, which occurs almost exclusively in adults. [3] Most frequently, the craniopharyngiomas affect both the intrasellar and suprasellar regions (70%), while the remaining 30% are exclusively suprasellar (20%) or intrasellar (10%) [1,2,3]. The severity of the clinical presentation largely depends on the size, location, and growth potential of the tumor. Neurologic disorders (such as headache and bitemporal hemianopsia) and endocrine deficiency (delayed growth and delayed puberty) are common complications of the craniopharyngiomas. By the time of the diagnosis, signs of endocrine dysfunction are noted in more than 80% of the patients, [3] and growth hormone deficiency constitutes the most common endocrine problem. Less frequent endocrine problems are FSH/LH (40%) or ACTH/TSH (25%) deficiency. [1,3] Furthermore, in the pediatric population, hydrocephalus may occur in 41% to 54% of all children diagnosed with craniopharyngioma. The location and extension of the craniopharyngiomas are critical factors in the development of clinical symptoms. Pre-chiasmatic lesions usually result in optic nerve atrophy, progressive decrease in visual acuity, and visual field abnormalities, while retrochiasmatic lesions associate with hydrocephalus and signs of intracranial hypertension (such as papilledema and horizontal diplopia). Intrasellar lesions, on the other hand, most frequently result in headache and endocrine abnormalities. [3,5] The craniopharyngiomas have a very characteristic appearance in the computed tomography and magnetic resonance imaging, allowing a correct preoperative differential diagnosis from other tumors that may affect the same region. The craniopharyngiomas frequently show solid, cystic, and calcified components, which constitute critical radiological clues. Usually, the cystic component is the most

important part of the tumor: the signal intensity is highly variable, as it depends on the chemical and physical properties (such as protein concentration) of its content. [1] With the computed tomography, it is possible to detect calcifications and also evaluate the bone anatomy. The magnetic resonance is particularly useful for topographic and structural studies, as it shows the anatomical relationships between the tumor, vascular structures, and the optic apparatus; therefore, it is essential for planning surgical interventions. [3,6] The resection of the craniopharyngiomas may be classified (as per the intraoperative impression of the neurosurgeon) in (1) gross total resection (GTR), when mere than 95% of the tumor is successfully resected; (2) subtotal, when more than 70% of the tumor is removed; and (3) partial, when less than 50% of the tumor is resected. [3,7,8] In small, intrasellar tumors, a gross total resection is achieved in the vast majority of the cases, and therefore no additional treatment is needed. In cases of subtotal or partial gross resection – which frequently occurs in craniopharyngiomas affecting the extrasellar area – the treatment may be complemented by adjuvant radiotherapy. [1] The morbidity of the surgical resection depends vastly on the size and aggressiveness of the tumor, but the surgical approach and the experience of the surgical team are also considered prognostic factors. The risks of damaging the hypothalamus are higher in invasive tumors resected through a transcranial approach. [1,9] Nonetheless, although the EETA associated with a lesser risk of complications, the incidence of endocrine dysfunction is high in both (transcranial and endonasal) approaches. [9] Therefore, patients subjected to craniopharyngioma resection are later followed by an endocrinologist. [10] To increase the chances for optimal results using the EETA for craniopharyngioma resection, it is important that the anatomy (spatial relationship of the posterior wall of the sphenoid sinus and the anterior/posterior walls of the sella turcica) and pneumatization of the sphenoid sinus are studied preoperatively. The pneumatization of the sphenoid sinus was classified by Hammer & Radberg, [11] in 1961, in three types: (1) conchal: the sphenoidal sinuses are very small and separated from the sella turcica by a thick bone wall of ~10mm; (2) presellar: the posterior boundary of the sphenoid sinus does not extend posterior to the line of fusion of the presphenoid and postsphenoid portions of the body of the sphenoid; and (3) sellar: the anterior wall and the floor of the sella turcica protrude into the sphenoidal cells.

The endoscopic endonasal transsphenoidal approach (EETA) is not as widely used in children as in adults. Initially, authors raised objections regarding the feasibility of performing an endoscopic approach to resect craniopharyngiomas in children, considering that the surgical anatomy (size of the nasal cavity and pneumatization of the sphenoid sinuses) in this population might be less favorable for a transsphenoidal procedure. Consequently, the literature available in the subject consists of only a limited number of studies, [4.12] which include only a small number of patients. Moreover, in those studies, the authors used the EETA mostly in cases of sellar and infradiaphragmatic lesions. [4] Therefore, the objective of this study is to analyze our series of pediatric patients subjected to craniopharyngioma surgery using the EETA.

2.

METHODS

From the Institute of Pediatric Oncology (IOP/GRAAC) of the Universidade Federal de São Paulo / Escola Paulista de Medicina (UNIFESP / EPM), We retrospectively reviewed the charts and medical records of 20 children diagnosed with craniopharyngioma who were subjected to surgical resection using the EETA, from 2007 to 2017. From the charts, we collected demographic information, results of imaging tests (size and extension of the tumor), and information regarding the surgical procedure and postoperative complications. All EETA surgeries were performed by a surgical team comprising of an otolaryngologist and a neurosurgeon. In those procedures, the surgical team used similar microsurgical dissection techniques using the endoscopic view (Video 1). The surgical steps used in all procedures were as follows: initially, we performed nasal vasoconstriction by placing sterile cotton strips saturated with a solution of adrenaline at a concentration of 1:1.000 in both nasal cavities. To avoid systemic complications of using a high concentration of adrenaline in younger children, the excess of adrenaline was squeezed off the cotton strips before their introduction in the nasal cavity. Then, a 0o rigid endoscope (diameter=4mm) attached to a high-definition (HD) camera was positioned in the surgical field and was used in the subsequent surgical steps. We did not experience surgical limitations with the use of a larger (4mm) endoscope in any of the patients. Using the technique described by Hadad et al., [13] we dissected a vascular pedicled nasoseptal flap, which was later used to reconstruct the skull base defect at the end of the surgery. In younger children, the dissection of the nasoseptal flap was more

challenging; however, in those cases, we performed the anterior mucosal incision in the region of the transition between the skin and mucosa, and we extended the posterior incision towards the lateral aspect of the choanal arch, close to the origin of its vascular irrigation in the sphenopalatine foramen. Using such a larger flap, we managed to adequately cover the region of the planum sphenoidale. Considering that the pneumatization of the clival recess of the sphenoid sinus in children is not as welldeveloped as in adults, the nasoseptal flap we dissected successfully reached and covered the whole defect, even in the anterior region. The sphenoid sinuses were opened and communicated, and the mucosal lining of the sphenoid sinuses was removed entirely; then, the sellar floor was drilled using a 3mm diamond burr (Fig. 1). If the lesion extended to the suprasellar region, we also drilled the planum sphenoidale. Then, we thoroughly dissected the tumor, carefully preserving the important adjacent neurovascular structures (pituitary stalk, optic chiasm, and superior hypophyseal and anterior cerebral arteries). The skull base was reconstructed in multiple layers, using fat graft, fascia lata graft, and also the vascular pedicled nasoseptal flap. The use of intradural fat to fill void spaces is not consensual in the literature; therefore, we only used the fat grafts in cases where – after the resection of the tumor – there was a suffiiciently wide cisternal space allowing the placement of the fat graft without compression of extrasellar structures. We did not use lumbar drains in any of the patients in our casuistic. Postoperative fistulae were surgically approached and sealed at the earliest opportunity. At the end of the surgery, we used a urethral catheter to support the nasoseptal flap. The balloon was placed in the posterior region of the nasal cavity and it was kept inflated for 3-5 days.

3. RESULTS

Among the 20 patients included in this study, 17 (85%) underwent EETA as the primary procedure, and three (15%) underwent EETA for relapsing craniopharyngioma following a previous transcranial approach. Twelve (60%) were women, and eight (40%) were men. In 12 (60%) patients, the tumors affected suprasellar areas, three (15%) extended to the third ventricle, and the remaining five (25%) were located only in the sellar area. The majority of these tumors (n=15; 75%) were both cystic and solid in their composition, and five (25%) were cystic. Four (20%) of the patients had visual problems prior to the surgery: two had amaurosis affecting the right eye due to tumor

compression; one had a bilateral visual acuity decrease due to tumor compression of the optic chiasm; and one had a bilateral decrease in the visual field due to compression of the optic chiasm and optic nerve. Table 1: Demographic, clinical, and surgical information of the 20 patients with craniopharyngioma who underwent EETA resection. ID Age, sex.

EETA 1st

Tumor location

Type

Resection

Postop fistula

Endocrine problems

Relapsing. Visual tumor problems

Sellar

Solid, cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Cystic

Complete

No

Panhypo

No

No

Complete

No

Panhypo

No

No

Subtotal

No

Panhypo

Yes

Yes

Complete

No

No

No

No

Subtotal

No

Panhypo

No

No

Complete

No

No

No

No

Subtotal

No

No

No

No

Complete

No

No

No

No

Complete

No

No

No

No

Subtotal

No

No

No

No

Complete

No

No

No

No

Complete

No

No

No

No

Subtotal

No

Panhypo

Yes

Yes

Complete

No

Panhypo

No

No

Complete

No

Panhypo

No

No

1

4y7m, F

2

16y13d, M 1st

Sellar/Suprasellar

3

5y11m, F

1st

Sellar/Suprasellar

4

4y10m, M

1st

Sellar/Suprasellar

5

11y, F

1st

Sellar/Suprasellar

6

7y, M

1st

Sellar/Suprasellar

7

7y4m, M

1st

Sellar/Suprasellar

8

11y, F

1st

Sellar/Suprasellar

9

9y, F

1st

Sellar/Suprasellar

10

12y, F

1st

Sellar/Suprasellar

11

5y4m, M

1st

Sellar/Suprasellar

12

13y, F

1st

Sellar/Suprasellar

13

3y, M

1st

Sellar

14

18y, M

15

13y, F

2nd Sellar/3rd ventricule 1st Sellar

16

9y4m, F 2nd

Sellar

Cystic

Complete

No

Panhypo

No

No

Sellar

Cystic

Complete

Yes

No

No

Yes

17

10y5m, F

1st

18

10y3m, F

1st Sellar/3rd ventricle

Cystic

Complete

No

Panhypo

No

No

19

11y1m, F

1st

Partial

No

Panhypo

Yes

Yes

20

7y4m, M

2nd Sellar/3rd ventricle

Solid cystic Cystic

Complete

No

Panhypo

No

No

Sellar/Suprasellar

We obtained a gross total resection (GTR; >95% of the tumor removed) in 14 (70%) patients (Fig. 2), subtotal (>70% of removal) in five (25%), and partial (less than 50% of the tumor removed) in one (5%). The six patients with either subtotal or partial gross resections underwent adjuvant radiotherapy. Regarding the postoperative complications, one (5%) patient had a cerebrospinal fistula, which was successfully treated with a further reconstruction of the skull base. None of the patients had postoperative infections. The patients underwent MRI testing to observe whether the findings would match the intraoperative classification of the surgical resection (total, subtotal, and partial). The MRI findings matched the intraoperative impression regarding degree of tumor resection in all patients. The follow-up period ranged from 2 to 9 years (mean=5.3 years). During the follow-up, 11 (55%) patients developed panhypopituitarism. Three (15%) of the patients were later diagnosed with relapsing tumors, all of which have had either subtotal (n=2) or partial (n=1) surgical resections. In two of those patients with relapsing tumors, the lesion previously affected suprasellar areas, and only in 1 the tumor was exclusively sellar. None of the patients who did not have visual abnormalities before the surgery developed any visual symptom, and those did not improve nor worsened postoperatively in patients who already have those visual problems.

4.

DISCUSSION

In our study, we demonstrated the results of craniopharyngioma resection using the EETA in 20 patients, 17 of which as a primary procedure, and in three patients as a secondary procedure after relapsing tumor following a primary transcranial resection. The study of Jane Jr. et al. [12] had a similar casuistic as ours, as 11 (50%) of their 22 patients underwent EETA as a primary procedure and the remaining 11 after a relapsing tumor. In cases where a gross total resection (GTR) was not achieved, patients were subjected to adjuvant radiotherapy, as recommended by several other studies. [3,10,12] In our study, we achieved a gross total resection (GTR) in 70% of the patients. Our results are similar to those reported by Stam et al. [3] (66.7%), Giorgio Frank et al. [2] (70%), Jane Jr. et al. [12] (68%) and Locatelli et al. [10] (81.5%). The frequency of subtotal resection we found (25%) was also similar to previous studies (7.5% - 18%). A

partial resection (<50% of resection) was observed in only one of our patients (5%), which also matches the observations of other authors who used EETA for craniopharyngioma resection – in the literature, the prevalence of partial resection following EETA ranged from 5% to 20%. Therefore, our results agree with previous observations showing that the EETA is a practical surgical approach for craniopharyngioma resection in children, as it associates with high rates of GTR. Regarding postoperative complications, our results showed that only 1 (5%) out of 20 patients subjected to craniopharyngioma resection using EETA had complications, which was a cerebrospinal fluid leak. Other studies in this regard also showed similar results: the incidence of postoperative cerebrospinal fistula ranged from 7.7% to 30%. [2,3,10] The vascular pedicled nasoseptal flap we used in our surgical procedures was initially described by Hadad et al., [13] in 2006 – the authors reported the results of the surgical technique in 44 adult patients (22-74 years old). Over the years, the use of the vascular pedicled nasoseptal flap was reported by several different authors, who demonstrated that it constitutes a safe method to reconstruct cranial base defects, even in children. Eleven of our patients (55%) developed panhypopituitarism after surgery. Our results were similar to what reported by Jane Jr. et al. (67%). [12] In this regard, Stam et al. [3] and Locatelli et al. [10] demonstrated that patients with preoperative panhypopituitarism might regain the endocrine hypophysis function after surgery, which was not observed in our casuistic. The presence of relapsing lesions following EETA craniopharyngioma resection we found in our study (15%) in the ~120-month follow-up period was similar to what reported by Jane Jr. et al. [12] – in their study, four patients (18%) developed relapsing lesions in the 82-month follow-up period. The authors also observed that – among patients with subtotal or partial resection – the frequency of relapsing tumors was higher as compared with patients with complete tumor removal (28.5% versus 13%). Several authors demonstrated that – among patients with preoperative visual problems secondary to a craniopharyngioma – the tumor resection using EETA led to improvements in either the visual acuity or visual field in 64%-93% of the patients. [3,12,14,15] In our casuistic, we did not observe significant improvement or worsening of visual problems among the patients who had visual problems before the surgery. The lack of visual improvements we observed postoperatively was probably caused by a

delay in the diagnosis and treatment, which is a significant inherent problem of the public health system of our country. Furthermore, it is necessary to take into consideration that comparisons between case series are somewhat questionable, considering that the tumors are heterogenous in their location, aggressiveness, and extension, and therefore the postsurgical results may vary significantly according to the characteristics of the studied population. It has been previously observed that there are no differences in the rates of postoperative endocrine problems between patients subjected to either transcranial or EETA craniopharyngioma resection. [3] However, the mortality rates in patients subjected to transcranial craniopharyngioma resection are higher than those demonstrated by recent studies using EETA (2.5% versus 0.0%). [3]

5.

CONCLUSION

Our results showed that the EETA is a safe and effective approach for removing craniopharyngiomas in children, as it associated with low operative morbidity and complication rates. Also, our data demonstrated that the EETA may be performed regardless of the size of the nasal cavity, pneumatization of the sphenoid sinuses, and location or extension of the tumors.

6.

ACKNOWLEDGEMENT

Department of Otorhinolaryngology and Head and Neck Surgery, Federal University of São Paulo - UNIFESP Discipline of Neurology and Neurosurgery, Federal University of São Paulo UNIFESP Institute of Pediatric Oncology - IOP / GRAACC / UNIFESP

7. [1]

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Figure legends

Fig. 1: An intraoperative photograph of a craniopharyngioma resection using the endoscopic endonasal transsphenoidal approach. (Bas A): Basilar artery; (SCA): superior cerebellar artery; (CN III) third cranial nerve; (PCA): posterior cerebral artery; (*) craniopharyngioma. Fig. 2: Pre- (A) and postoperative (B) sagittal MRI showing the gross total removal of a craniopharyngioma in a 4-year-old girl (Case 1)

Video legend

Video 1: Subtotal resection of a craniopharyngioma (using the endoscopic endonasal transsphenoidal approach) in a 3-year-old female child who had a sellar tumor with suprasellar extension.

Table 1: Demographic, clinical, and surgical information of the 20 patients with craniopharyngioma who underwent EETA resection. ID Age, sex.

EETA 1st

Tumor location

Type

Resection

Postop fistula

Endocrine problems

Relapsing. Visual tumor problems

Sellar

Solid, cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Solid cystic Cystic

Complete

No

Panhypo

No

No

Complete

No

Panhypo

No

No

Subtotal

No

Panhypo

Yes

Yes

Complete

No

No

No

No

Subtotal

No

Panhypo

No

No

Complete

No

No

No

No

Subtotal

No

No

No

No

Complete

No

No

No

No

Complete

No

No

No

No

Subtotal

No

No

No

No

Complete

No

No

No

No

Complete

No

No

No

No

Subtotal

No

Panhypo

Yes

Yes

Complete

No

Panhypo

No

No

Complete

No

Panhypo

No

No

1

4y7m, F

2

16y13d, M 1st

Sellar/Suprasellar

3

5y11m, F

1st

Sellar/Suprasellar

4

4y10m, M

1st

Sellar/Suprasellar

5

11y, F

1st

Sellar/Suprasellar

6

7y, M

1st

Sellar/Suprasellar

7

7y4m, M

1st

Sellar/Suprasellar

8

11y, F

1st

Sellar/Suprasellar

9

9y, F

1st

Sellar/Suprasellar

10

12y, F

1st

Sellar/Suprasellar

11

5y4m, M

1st

Sellar/Suprasellar

12

13y, F

1st

Sellar/Suprasellar

13

3y, M

1st

Sellar

14

18y, M

15

13y, F

2nd Sellar/3rd ventricule 1st Sellar

16

9y4m, F 2nd

Sellar

Cystic

Complete

No

Panhypo

No

No

Sellar

Cystic

Complete

Yes

No

No

Yes

17

10y5m, F

1st

18

10y3m, F

1st Sellar/3rd ventricle

Cystic

Complete

No

Panhypo

No

No

19

11y1m, F

1st

Partial

No

Panhypo

Yes

Yes

20

7y4m, M

2nd Sellar/3rd ventricle

Solid cystic Cystic

Complete

No

Panhypo

No

No

Sellar/Suprasellar