Journal of Clinical Neuroscience xxx (2015) xxx–xxx
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Clinical Study
Third ventricular meningiomas Puxian Li a,b, Xingtao Diao a, Zhiyong Bi b, Shuyu Hao b, Xiaohui Ren b, Junting Zhang b,⇑, Jun Xing c a
Department of Neurosurgery, Laiwu Hospital, Taishan Medical University, Laiwu 271100, China Department of Neurosurgery, Beijing Tian Tan Hospital, Capital Medical University, Beijing 100050, China c Department of Medical, Laiwu Hospital, Taishan Medical University, Laiwu 271100, China b
a r t i c l e
i n f o
Article history: Received 9 February 2015 Accepted 1 May 2015 Available online xxxx Keywords: Clinical features Microsurgery Pathology Radiology Third ventricular meningioma Ventricular meningioma
a b s t r a c t We report 13 patients with third ventricular meningiomas (TVM) and discuss the clinical, radiological, pathological and surgical features, as well as follow-up of these tumors. TVM are rare intracranial tumors, and because of this, there are few reports in the literature. Of 11,600 intracranial meningiomas that were surgically treated and pathologically confirmed at Beijing Tian Tan Hospital over a period of 10 years (2003–2013), 13 TVM were selected for a retrospective review. We recorded the clinical, radiological, pathological, and surgical data and statistically analyzed the preoperative, postoperative and 6 month postoperative Karnofsky performance scale (KPS) scores. TVM represented 0.11% of intracranial meningiomas. Radiologically, TVM were divided into three groups: anterior (n = 3), posterior (n = 3), and entire third ventricle (n = 7). Three patients (23.1%) were misdiagnosed preoperatively. Total removal was achieved in 61.5% (8/13) of patients, and subtotal resection was achieved in 38.5% (5/13). Pathologically, the tumors were World Health Organization (WHO) Grade I in 11 patients (84.6%) and WHO Grade II in two (15.6%). There were no statistically significant differences in the preoperative, postoperative, or 6 month postoperative KPS scores (F = 0.814; p = 0.401). TVM without dural attachments are rare neoplasms that should be differentiated from choroid plexus papilloma, craniopharyngioma, and pineocytoma. Surgery is the optimal treatment and may result in a favorable prognosis, and understanding of the radiological subtype can help with the choice of surgical approach. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Intraventricular meningiomas are rare tumors, most of which are located in the lateral ventricle. They lack dural attachments and account for 0.5–5% of all intracranial meningiomas [1,2]. Third ventricular meningiomas (TVM) are extremely uncommon, representing only 0.1–0.18% of intracranial meningiomas [2–4]. An extensive review of the literature in 2003 found only 83 reported patients with TVM [5], and, to our knowledge, only seven further patients have been reported since 2003 in the English language literature. Therefore, a total of only 90 TVM have been reported to date. Most of these are from case reports or are sporadic cases in series of intraventricular meningiomas. Due to their deep location and proximity to crucial neurovascular structures, surgery for TVM is challenging. The morbidity and mortality rates were relatively high in early surgical reports. In 1978, Avman et al. [3] summarized 14 surgical TVM patients from the literature. Seven of these patients died after surgery, and five
⇑ Corresponding author. Tel.: +86 10 67098431; fax: +86 10 67051377. E-mail address: [email protected] (J. Zhang).
survived with severe neurological deficits. However, with advances in microsurgical techniques, perioperative equipment and postoperative intensive care, this situation has greatly improved. In 2014, Karki et al. [6] summarized nine patients with TVM. In their series, two patients died after surgery, but all others had good outcomes. Due to the rarity of the disease and the surgical challenges, further research is still needed to illuminate this rare entity. We retrospectively reviewed all TVM surgically treated and pathologically confirmed at Beijing Tian Tan Hospital over 10 years, from 2003–2013. Thirteen patients were identified, and the clinical, radiological, and pathological features, as well as surgical approaches and outcomes, were evaluated. To our knowledge, this is the largest single institution series of TVM.
2. Materials and methods A review of medical records identified 11,600 patients who underwent surgical treatment of pathologically confirmed intracranial meningiomas at Beijing Tian Tan Hospital during the study period. TVM were selected for analysis through a retrospective review of clinical, radiological, surgical, pathological and
http://dx.doi.org/10.1016/j.jocn.2015.05.025 0967-5868/Ó 2015 Elsevier Ltd. All rights reserved.
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
follow-up records. Prior written and informed consent was obtained from every patient, and the study was approved by the Ethics Review Board of Beijing Tian Tan Hospital. Clinical information was collected, including age and sex, symptoms and signs, the duration from symptom onset to admission, and preoperative diagnosis. The radiologic data included density on CT scans, intensity of T1- and T2-weighted enhancement on MRI, tumor location, tumor size, tumor shape, and the presence of hydrocephalus (based on MRI). The tumors were divided into three types according to location: anterior, posterior and entire third ventricle (using the massa intermedia as a boundary). Tumor size was defined as the maximum diameter on MRI. The surgical findings included the surgical approach, tumor color, tumor texture, tumor border, tumor blood supply, extent of tumor removal, blood loss during the operation, surgical time, surgical outcomes, and surgical complications. The extent of tumor removal was classified as total, subtotal or partial, based on the surgical records and postoperative MRI. The pathological type was determined according to the 2007 World Health Organization (WHO) classification of tumors of the central nervous system [7]. The follow-up data regarding complications, recurrences, treatment after discharge, and patient deaths were collected. Karnofsky performance scale (KPS) scores were also evaluated preoperatively, postoperatively and at 6 months after surgery. Statistical analyses were performed using SPSS software (version 17.0; IBM Corporation, Armonk, NY, USA). Statistical significance was defined as p < 0.05.
3. Results 3.1. Incidence and clinical features The incidence of ventricular meningiomas and TVM was 2.1% (240/11,600) and 0.11% (13/11,600) of all meningiomas, respectively. The clinical features of TVM are summarized in Table 1. Of the 13 TVM patients, there were seven males and six females. The age at hospital admission was 31.3 ± 18.3 years (mean ± standard deviation [SD]; range: 7–56). The duration from symptom onset to admission was a median of 12 months (range: 3 months to 5 years). In terms of the major symptoms and signs, eight patients presented with headaches, four with visual deficits, four with somnolence, three with ataxia, and three with limb weakness. Hearing loss, urinary incontinence, memory defect, and hormone abnormalities occurred in two patients each. Upgaze palsy, dysgraphia, amenorrhea, and diabetes insipidus occurred in one patient each. There were no patients with recurrent tumors or neurofibromatosis, and no patients underwent radiotherapy before hospital admission. Three patients (23.1%) were misdiagnosed preoperatively as having choroid plexus papilloma, craniopharyngioma, or pineocytoma (Fig. 1).
CT scans were available for seven patients. All tumors were hyperdense, and three had calcification. MRI examinations were performed for all patients. Seven tumors were isointense on T1and T2-weighted images. One tumor each was isointense on T1- and isohypointense on T2-weighted images, isointense on T1and hyper-hypointense on T2-weighted images, isohypointense on T1-weighted and hypointense on T2-weighted images, isointense on T1- and slightly hyperintense on T2-weighted images, slightly hypointense on T1- and isohyperintense on T2-weighted images and hypointense on T1- and T2-weighted images. MRI demonstrated homogenous enhancement in seven tumors, and heterogeneous enhancement in six. 3.3. Surgical findings and pathological types The surgical findings are summarized in Table 1, 3. Before surgery, one patient underwent placement of a ventriculoperitoneal shunt because of obstructive hydrocephalus. To remove the tumor, a right frontal craniotomy with a transcallosal transforniceal approach was performed in eight patients. A right frontal craniotomy with a transcallosal transventricular transchoroidal approach was performed in two patients, a right frontal craniotomy with a transcortical transventricular transchoroidal approach was performed in two, and an occipital transtentorial approach was used in one. Most of the tumors were gray–white in color (n = 9), three were gray–red, and one was pink. The tumor texture was tenacious in four, a mixture of firm and tenacious in three, soft in three, a mixture of soft and tenacious in one, and a mixture of firm, tenacious and soft in one patient. Seven tumors had a rich blood supply and six had a moderate blood supply. All tumors, except one, were well defined from the surrounding tissues. Total removal was achieved in eight (61.5%), and subtotal resection was achieved in five (38.5%) patients. The surgical duration was 7 ± 2.3 hours (mean ± SD; range: 4– 13). The mean blood loss during surgery was 500 ml (range: 200–2000). Eight patients had a drainage tube inserted, and all tubes were removed 1–3 days postoperatively. Regarding postoperative complications, electrolyte disturbances were found in six, hormone abnormalities in three, and subdural fluid accumulation in one patient. Diabetes insipidus, mutism, obstructive hydrocephalus, and intracranial infection occurred in two patients each. Two patients with obstructive hydrocephalus underwent a ventriculoperitoneal shunt placement after tumor removal. All complications were resolved before discharge, except in two patients who had hormonal abnormalities, one with diabetes insipidus who needed supplementary medication, and one with an intracranial infection who was discharged before the infection was controlled. The pathological subtypes are shown in Table 1. There were four fibrous, three lymphoplasmacyte-rich, and three transitional subtypes. Meningothelial, chordoid, and fibrous tumors with brain invasion were observed in one patient each (Fig. 5, 6). WHO Grade I tumors occurred in 11 patients (84.6%), and WHO Grade II in two (15.6%).
3.2. Radiological features 3.4. KPS and follow-up The radiological features are summarized in Table 1, 2. In terms of tumor location, there were three anterior, three posterior, and seven entire third ventricle type tumors (Fig. 2–4). Three tumors bulged into the bilateral lateral ventricles, two into the unilateral lateral ventricle, and two involved the septum pellucidum. In terms of the tumor shape, six were spherical, three were lobulated, and two were irregular. Dumbbell and cylindrical shapes were observed in one patient each. A total of nine patients had hydrocephalus, and nine had brain edema. The maximal tumor diameter was 5.1 ± 1.8 cm (mean ± SD; range: 2.3–8.2).
Data regarding the KPS are shown in Table 1. The median preoperative KPS was 80 (range: 70–100), and was unchanged postoperatively (median 80; range: 30–100). The median KPS 6 months after surgery was 90 (range: 0–100). There were no significant differences among the three groups on the test of repeated measures (F = 0.814; p = 0.401). All patients were followed up for 65.3 ± 42.9 months (mean ± SD; range: 3–129). Two patients had hormonal abnormalities, and one had diabetes insipidus, which resolved during the
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
Symptoms Patient Age (years), sex
Duration Preoperative (months) diagnosis
Tumor location Tumor in third ventricle size (cm)
Surgical approach
Extent of tumor removal
Pathological type
WHO KPS Grade Preop Postop 6 months postop
Transcallosal transventricular transchoroidal Transcallosal interforniceal Transcallosal interforniceal Occipital transtentorial Transcallosal interforniceal Transcallosal interforniceal Transcallosal transventricular transchoroidal Transcallosal interforniceal Transcortical transventricular transchoroidal Transcallosal interforniceal Transcortical transventricular transchoroidal Transcallosal interforniceal Transcallosal interforniceal
Subtotal
Transitional
I
70
90
100
Total
70
80
90
Total
Lymphoplasmacyte- I rich Meningothelial I
90
100
100
Subtotal
Fibrous
I
70
80
100
Total
80
90
90
Total
Lymphoplasmacyte- I rich Fibrous I
80
70
80
Subtotal
Transitional
I
80
80
100
Total
Fibrous
I
70
70
90
Total
Lymphoplasmacyte- I rich
80
70
90
Subtotal
80
70
70
Total
Fibrous, infiltrating II brain tissue Fibrous I
70
30
0
Subtotal
Transitional
I
100
100
100
Total
Chordoid
II
90
90
90
1
7, M
Headache, nausea, vomiting, gait ataxia, dysgraphia, 13 papilledema
Choroid plexus papilloma
Entire
7.4
2
28, F
12
Craniopharyngioma Entire
6.2
3
8, M
Headache, visual deterioration, memory deficit, amenorrhea, optic atrophy Headache, nausea, vomiting
2
Meningioma
Anterior
3
4
43, F
Headache, ataxia, upgaze palsy, left limb weakness
24
Meningioma
Posterior
5
5
30, M
12
Meningioma
Entire
5
6
46, F
Headache, visual deterioration, bilateral temporal hemianopsia, somnolence, diabetes insipidus Visual deterioration
3
Pineocytoma
Posterior
2.3
7
15, M
Headache, vomiting, right sided tinnitus, hearing loss 25
Meningioma
Entire
6.4
8
56, F
Meningioma
Entire
6.1
9
39, M
Right limb weakness, somnolence, urinary 13 incontinence Visual deterioration, bilateral temporal hemianopsia 60
Meningioma
Anterior
3.5
10
56, F
Somnolence
Meningioma
Posterior
5
11
12, M
Gait ataxia, left limb weakness, urinary incontinence 26
Meningioma
Entire
8.2
12
16, M
Headache
Meningioma
Entire
5.7
13
51, F
Headache, somnolence, memory defect, hearing loss 12
Meningioma
Anterior
3
6
3
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
Table 1 Clinical, radiological, and pathological features of 13 patients with TVM
KPS = Karnofsky performance scale, Postop = postoperative, Preop = preoperative, TVM = third ventricular meningioma, WHO = World Health Organization.
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Fig. 1. Patient 1, 2 and 6 were misdiagnosed with choroid plexus papilloma, craniopharyngioma, and pineocytoma, respectively. Patient 1: A lobular third ventricular tumor showed isointensity on (A axial) T1- and (B axial) T2-weighted MRI, and (C axial, D sagittal) homogeneous enhancement on the enhanced T1-weighted MRI; the tumor bulged into the right lateral ventricle. Patient 2: A dumbbell-shaped third ventricular tumor demonstrated (A axial) T1-weighted isointensity, (B axial) slight T2-weighted hyperintensity and (C axial, D sagittal, E coronal) homogeneous enhancement on the enhanced T1-weighted MRI. Patient 6: A spherical third ventricular lesion showed (A axial) high density and calcification on CT scan, and (B axial, D sagittal) iso- to hypointensity on the T1-weighted MRI, (C axial) hypointensity on the T2-weighted MRI, and (E axial) inhomogeneous enhancement on the enhanced T1-weighted MRI.
follow-up period. Three patients died during follow-up. One patient died of an intracranial infection 3 months after surgery, which was considered to be related to the surgery, one died of renal failure 2 years after surgery, and one died of gastric carcinoma 8 years after the meningioma surgery. Seven patients were able to continue with their normal studies or work, and three were able to live independently. No patient underwent radiotherapy or suffered a tumor recurrence. 4. Discussion TVM are a rare location of meningioma, and they can be easily misdiagnosed due to their atypical location and lack of dural attachment. Surgery for TVM is challenging due to the deep location and proximity to crucial neurovascular structures. Most of the reported patients are in case reports or are sporadic cases included in intraventricular meningioma series. From 2003–2013, 11,600 meningiomas were surgically treated in our hospital, 13 of which were confirmed to be TVM. To the best of our knowledge, this is the largest single institution series of TVM. 4.1. Incidence and origin of TVM The incidence of TVM is extremely low, with only 90 patients reported in the literature to date, including unspecified falcotentorial meningiomas [8–12]. The incidence of TVM is 0.1–0.18% of all intracranial meningiomas [2–4]. In the present series, only 13 TVM without dural attachment were found among the 11,600 intracranial meningiomas that were surgically treated and pathologically
confirmed at Beijing Tian tan Hospital over 10 years (2003– 2013), yielding an incidence of 0.11% of all meningiomas. It is known that most intracranial meningiomas occur in adults, with a female predominance. However, in our series, 31% (4/13) of TVM occurred in patients 6 16 years of age, with an almost equal male to female ratio. This finding is in accordance with most studies of TVM, which have reported a slightly higher incidence in males and the pediatric age group [3,9,12,13]. A comparison of previous studies and the present study of TVM is shown in Table 4. Because of a lack of symptoms early in the course of disease, or because of anticipated surgical challenges, some tumors can grow to a large size. The largest tumor in our series measured 8.2 cm, and most TVM were WHO Grade I (84.6%), with only two Grade II (15.4%). Among the WHO Grade II TVM, one was a chordoid meningioma, being only the third tumor of this type and location to have been reported [14,15]. Additionally, the fibrous meningioma of the third ventricle with brain invasion is the first to be reported, to our knowledge. TVM may originate from the choroid plexus, the tela choroidea of the velum interpositum, the tenia fornicis, or the connective tissue stroma of the pineal body [3,8–13,16]. Most authors suggest that the tela choroidea of the velum interpositum is the primary origin of TVM. During the initial stage of embryonic development, only one layer of the pia mater extends over the roof of the third ventricle, and when the corpus callosum extends posteriorly, it carries with it a layer of pia on its inferior surface, above the level of the choroid fissure. This overlies the original single pia layer, fusing with it to form the tela choroidea [9]. The velum interpositum is the potential space between the
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx Table 2 Radiological features of 13 patients with TVM Characteristics Location Anterior third ventricle Posterior third ventricle Entire third ventricle Bulging into left lateral ventricle Bulging into right lateral ventricle Bulging into bilateral lateral ventricles Bulging into septum pellucidum Shape of tumor Spherical Lobulated Irregular Dumbbell Cylindrical Hydrocephalus Yes No Brain edema Yes No Tumor size (cm) Mean ± SD Range CT scan Hyperdensity Calcification N/A T1-/T2-weighted MRI Isointense T1 and T2 Isointense T1, isohypointense T2 Isohypointense T1, isohyperintense T2 Isohypointense T1, hypointense T2 Isointense T1, light hyperintense T2 Slightly hypointense T1, isohyperintense T2 Hypointense T1 and T2 Enhancement Homogenous Heterogeneous
n (%) 3 3 7 1 1 3 2
(23.1) (23.1) (53.8) (7.7) (7.7) (23.1) (15.4)
6 3 2 1 1
(46.2) (23.1) (15.4) (7.7) (7.7)
9 (69.2) 4 (30.8) 9 (69.2) 4 (30.8) 5.1 ± 1.8 2.3–8.2 7 (53.8) 3 (23.1) 6 (46.2) 7 1 1 1 1 1 1
(53.8) (7.7) (7.7) (7.7) (7.7) (7.7) (7.7)
7 (53.8) 6 (46.2)
N/A = not available, SD = standard deviation, TVM = third ventricular meningioma.
5
dorsal and ventral layers of the tela choroidea that contains the internal cerebral veins and medial posterior choroidal arteries. The velum interpositum, the two layers of the tela choroidea, and the body and crura of the fornices together form the roof of the third ventricle. The definition of the velum interpositum is often broadened to include the two layers of the tela choroidea, together with the velum interpositum proper [13]. In this study, we have used the broader term. Most TVM derive their blood supply from the medial posterior choroidal artery, but the lateral posterior choroidal artery, anterior choroidal artery, and even posterior pericallosal artery may contribute to the blood supply [8,9,12,13,15,17]. 4.2. Radiological type and its relationship to symptoms Previously, TVM have been divided into two radiological groups based on the involvement of the anterior and posterior parts of the third ventricle, and no line of demarcation was reported [4,8–13]. However, we found that some TVM occupied almost the entire third ventricle, so we divided the TVM into three groups: anterior, posterior, and entire (bounded by the massa intermedia). The anterior type TVM can compress the hypothalamus and optic tract, causing somnolence, memory deficits, hormonal abnormalities, diabetes insipidus or visual deficits. The posterior type may resemble pineocytomas and can compress the quadrigeminal plate, mesencephalon, cerebellum, or the medial and lateral geniculate bodies, leading to upgaze palsy (Parinaud’s syndrome), limb weakness, and gait ataxia, as well as visual or hearing deficits. The entire type can, therefore, have symptoms of both the anterior and posterior types. Tumor compression of the temporal lobe can cause language deficits, and compression of the fornix and hippocampus can cause memory loss. Mass effect and hydrocephalus can result in symptoms of increased intracranial pressure. Hydrocephalus alone can cause urinary incontinence as well as memory or visual deficits.
Fig. 2. Patient 9. Representative images of the anterior type third ventricular meningioma. A spherical third ventricular tumor showed mainly (A axial) high density on CT scan, and (B axial) iso- to hypointensity on T1-weighted MRI, (C axial) iso- to hyperintensity on T2-weighted MRI, and (D axial, E sagittal, F coronal) inhomogeneous enhancement on the enhanced MRI. (G axial) The postoperative T1-weighted MRI showed complete resection of the lesion. (H; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a lymphoplasmacyte-rich meningioma.
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Fig. 3. Patient 4. Representative images of the posterior type third ventricular meningioma. On MRI, the spherical tumor was (A axial) isointense on T1-weighted images, (B axial) isointense on T2-weighted images, and (C axial, D sagittal, E coronal) homogenous enhancement on the enhanced T1-weighted MRI, with obvious hydrocephalus.
Fig. 4. Patient 11. Representative images of the entire type third ventricular meningioma. The tumor primarily demonstrated (A axial) isointensity on T1- and (B axial) T2weighted images, and (C axial, D sagittal, E coronal) heterogeneous enhancement on the enhanced T1-weighted MRI. The tumor filled the third ventricle and bulged into the bilateral lateral ventricles and septum pellucidum, with obvious hydrocephalus.
4.3. Differential diagnosis of TVM TVM lack dural attachments and are easily misdiagnosed. Choroid plexus papilloma, craniopharyngioma, astrocytoma, ependymoma, pituitary adenoma and colloid cysts should be differentiated from the anterior and entire types of TVM. Germ cell tumors and pineocytoma should be differentiated from posterior TVM. In our series, three patients (23.1%) were misdiagnosed preoperatively as having choroid plexus papilloma, craniopharyngioma, and pineocytoma. Choroid plexus papilloma generally occurs in children and has an irregular and cauliflower-like radiographic appearance. MRI usually demonstrates T1-weighted hypointensity, T2-weighted hyperintensity and obvious enhancement. Craniopharyngiomas can occur at any age, but most develop in children and adolescents. Craniopharyngioma usually presents with symptoms of hypopituitarism and hypothalamic damage, and calcification and cystic changes can be seen on imaging, but many ventricular craniopharyngiomas have no calcification or cystic changes [18]. Pan et al. [19] reported that 35.3% of ventricular craniopharyngiomas were completely solid and that 47.1% lacked calcification. Pineocytomas are located in the pineal region and usually develop in adults. Patients may have symptoms of Parinaud’s syndrome and arrest of sexual development. Calcification may be seen on CT scans, and these tumors usually demonstrate T1-weighted isointensity or hypointensity, T2-weighted hyperintensity and homogeneous enhancement on MRI. Despite advanced radiographic techniques, TVM are often misdiagnosed as other tumors, and confirmation of the diagnosis requires histopathology. 4.4. Selection of surgical approach for TVM and microsurgery The choice of surgical approach for TVM depends on the tumor location, adjacent structures (especially the deep venous systems), patient status and the surgeon’s preferences. For the anterior type of TVM, surgical approaches include the anterior transcortical transventricular transchoroidal/transforminal approach, the anterior interhemispheric transcallosal interforniceal approach, the anterior interhemispheric transcallosal transventricular tran-
Table 3 Surgical findings in 13 patients with TVM Characteristics Surgical approach Transcallosal interforniceal Transcallosal transventricular transchoroidal Transcortical transventricular transchoroidal Occipital transtentorial Tumor color Gray–white Gray–red Pink Tumor texture Tenacious Firm and tenacious Soft Soft and tenacious Firm, tenacious and soft Tumor blood supply Rich Moderate Tumor border Well defined Poorly defined Extent of resection Total Subtotal Operation time (hours) Mean ± SD Range Blood loss during operation (mL) Median Range Drainage tube insertion Yes No Postoperative complications Electrolyte disturbance Hormone abnormality Diabetes insipidus Mutism Obstructive hydrocephalus Intracranial infection Subdural fluid accumulation
n (%) 8 2 2 1
(61.5) (15.4) (15.4) (7.7)
9 (69.2) 3 (23.1) 1 (7.7) 4 3 3 2 1
(30.8) (23.1) (23.1) (15.4) (7.7)
7 (53.8) 6 (46.2) 12 (92.3) 1 (7.7) 8 (61.5) 5 (38.5) 7 ± 2.3 4–13 500 200–2000 8 (61.5) 5 (38.5) 6 3 2 2 2 2 1
(46.1) (23.1) (15.4) (15.4) (15.4) (15.4) (7.7)
SD = standard deviation, TVM = third ventricular meningioma.
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
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Fig. 5. Patient 13. Images of a third ventricular chordoid meningioma. The spherical tumor was located in the anterior part of the third ventricle and showed (A axial) high density on CT scan, (B axial) isointensity on T1- and (C axial) T2-weighted MRI, and (D axial, E sagittal, F coronal) homogeneous enhancement on the enhanced T1-weighted MRI. (G axial) Postoperative MRI revealed total resection of the tumor. (H; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a chordoid meningioma.
Fig. 6. Patient 10. Images of a third ventricular fibrous meningioma with brain invasion. The tumor demonstrated (A axial) isointensity on T1-weighted MRI, (B axial) iso- to hypointensity on T2-weighted MRI, and (C axial, D sagittal, E coronal) heterogeneous enhancement on the enhanced T1-weighted MRI. (F axial) The postoperative CT scan showed complete tumor resection and the insertion of a drainage tube into the third ventricle. (G; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a fibrous meningioma with brain invasion.
schoroidal/transforminal approach, the subfrontal, pterional or anterior interhemispheric translamina terminalis approaches, or the anterior callosal section combined with the anterior interhemispheric translamina terminalis approach [2–5,10,14,17,20–26]. For the posterior type of TVM, surgical approaches include the anterior
transcortical transventricular transchoroidal approach, the anterior interhemispheric transcallosal interforniceal approach, the anterior interhemispheric transcallosal transventricular transchoroidal approach, the posterior interhemispheric transcallosal approach, the infratentorial supracerebellar approach, and the occipital
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
BI = brain invasion, F = female, M = male, N/A = not available, SD = standard deviation, TVM = third ventricular meningioma. a Sex information was not available for one patient.
Total (8); subtotal (5) Transcallosal interforniceal (8); transcallosal transventricular transchoroidal (2); transcortical transventricular transchoroidal (2); occipital transtentorial (1) 12 (3–60) 7:6 13 Present study
31.3 ± 18.3 (7–56)
N/A 6:2a 9 Karki et al.[6]
32.3 ± 24.8 (6–63)
7 (1–120) 11:6 17 Lozier et al.[13]
32.9 ± 17.6 (6–61)
N/A 11:11 22 Cabezudo et al.[4]
28.5 ± 17.9 (2–59)
Good (12); died 6 months postoperatively (1)
Good (7); died (2)
Meningothelial (1); atypical (1); chordoid (1); atypical-papillarymalignant (1); N/A (5) Fibrous (4); lymphoplasmacyte-rich (3); transitional (3); meningothelial with BI (1); chordoid with BI (1); fibrous with BI (1) Total (6); subtotal (1); debulking (1); N/A (1)
Total (13); subtotal (1); tumor not seen (1); N/A (2)
Fibrous (5); psammomatous (2); meningothelial (1); transitional (1); N/A (5) Fibrous (8); psammomatous (7); meningothelial (1); transitional (4); N/A (2) N/A Total (5); subtotal (1); N/A (8) 14 Avman et al.[2]
25.5 ± 17.0 (3–53)
7:7
24 (3–180)
Transventricular transforminal (3); anterior transcallosal (1); posterior transcallosal (2); N/A (8) Transventricular (11); anterior transcallosal (1); parieto-occipital (1); N/A (9) Infratentorial supracerebellar (4); occipital transtentorial (3); transcallosal (3); parieto-occipital (2); occipital (2); frontal (1); parietal (1); suboccipital (1) Transcortical transventricular (5); transcallosal (2); N/A (2)
Total (n = 13); subtotal (1); N/A (8)
Pathological type Extent of resection Surgical approach Symptom duration, median months (range) Sex, M:F Age, mean years ± SD (range) Patients, n Study
Table 4 Comparison of TVM features between previously reported studies and the present study
Survived with severe neurological deficits (5); died (7); N/A (2) Good (4); survived with neurological deficits (5); died (12); N/A (1) Good (4); survived with neurological deficits (8); died (2); N/A (3)
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Outcome
8
transtentorial approach [3,9,12,13,27]. In our opinion, for the entire type of TVM, the anterior transcortical transventricular transchoroidal approach, the anterior interhemispheric transcallosal interforniceal approach, or the anterior interhemispheric transcallosal transventricular transchoroidal approach is suitable, as these tumors are usually large. A subfrontal approach, involving opening the frontal sinus, may increase the risk of infection, cosmetic abnormalities, extensive frontal lobe retraction, and olfactory bulb disruption [18]. The pterional approach provides limited exposure and is not suitable for large third ventricle tumors. Shiramizu et al. [24] believed that the anterior interhemispheric translamina terminalis approach could be used for anterior and inferior tumors of the third ventricle, but as the dorsal part of anterior third ventricular tumors is hidden from the anterior corpus callosum, requiring an anterior callosal section, the optimal indication for the combined approach is the treatment of tumors growing anteriorly from the line joining the anterior ridge of the foramen of Monro and the cerebral aqueduct. The transventricular approach is fit for TVM with dilation of the lateral ventricle, or a significant intraventricular component. The approach is generally through the right ventricle, as the right side is usually the non-dominant hemisphere, unless the tumor has an obvious and large projection into the left ventricle, in which case a left ventricular approach should be used. When a transventricular approach is used for a transcortical procedure, the cortical incision may lead to postoperative seizures and subdural fluid collections [2]. The transforminal approach is suitable for smaller tumors located in the anterior part of third ventricle, particularly if there is enlargement of the foramen of Monro. Also, the surgical field can be enlarged by dissecting the choroidal fissure, so that the field of view is increased [28]. The occipital transtentorial approach is appropriate for posterior type TVM that are centered in the quadrigeminal cistern and displace the deep venous system inferiorly. If the tumor originates from the ventral leaf of the tela choroidea and displaces the internal cerebral veins dorsally, the infratentorial supracerebellar approach is suitable. If the tumor originates from the dorsal leaf of the tela choroidea, displaces the internal cerebral veins ventrally, and does not extend posteriorly to the splenium of the corpus callosum, the posterior interhemispheric transcallosal approach can be selected [13]. In our series, the anterior interhemispheric transcallosal interforniceal approach or anterior interhemispheric transcallosal transventricular transchoroidal approach was performed in 77% (10/13) of patients. We prefer these two approaches for four reasons. First, the interhemispheric transcallosal approach reaches the third ventricle via natural anatomical spaces and without a cortical incision. Second, the interhemispheric transcallosal approach is suitable for almost all third ventricular tumors, especially for large tumors (most tumors in our series were large). Third, in our series, most patients had enlargement of the lateral ventricles due to hydrocephalus, allowing a transventricular approach. Lastly, our senior author is familiar with those two approaches. During surgery involving the interhemispheric transcallosal approach, long microsurgery instruments should be prepared, such as the long scissor, long bipolar forceps, and long aspirator. It is important to protect the cortical bridging veins and deep venous system, especially the internal cerebral veins, otherwise significant edema can result. If the internal cerebral veins are occluded, disastrous consequences may occur. The length of the corpus callosum incision should be limited to no more than 2.5 cm, or mutism or disconnection syndrome may result [20]. In our series, the corpus callosum incision was limited to 2 cm. In order to avoid injuring crucial adjacent structures, such as the hypothalamus and the deep venous system, the tumor should be removed in a piecemeal manner. Tumor tissue may occasionally need to be left behind,
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
particularly in situations where the tumor is closely adherent to a vital adjacent structure.
4.5. Management of TVM Although surgery for TVM is challenging, it is the optimal treatment for these benign tumors. Relatively positive results were achieved in our series of TVM patients following surgery. Total removal was achieved in 61.5% (8/13), and subtotal resection was performed in 38.5% (5/13) of patients. Only one patient died as a result of surgery, and there were no statistically significant differences between preoperative, postoperative, and 6 month KPS scores. At follow-up seven patients were able to continue with their normal study or work, three were living independently, and two died of other diseases. It is important to perform a detailed preoperative clinical and radiological evaluation in order to prepare patients for surgery and to decide on the optimal surgical approach. The management of postoperative complications is also important, including timely CT scans to rule out intracranial hematomas, close monitoring of postoperative water and electrolyte balance, monitoring and appropriate treatment of endocrine disturbances, and treatment of intracranial infections with antibiotics and drainage of lumbar or cerebrospinal fluid. Most patients with hydrocephalus improve after surgery, but if resolution does not occur, ventriculoperitoneal shunting can be performed. Gamma Knife (Elekta AB, Stockholm, Sweden) or photon radiation can be performed for the treatment of residual and recurrent TVM. Large field radiation is not suitable for these tumors because of their proximity to critical adjacent structures. Chemotherapy for these tumors is controversial, and no adjuvant treatment is needed for completely resected TVM.
5. Conclusion TVM without dural attachment are rare neoplasms, which should be differentiated from choroid plexus papilloma, craniopharyngioma, and pineocytoma. Surgery for TVM is full of challenges because of the deep location and crucial adjacent neurovascular structures. Nevertheless, surgery remains the optimal treatment and may result in a favorable prognosis. Definition of the radiological type and location can aid the choice of surgical approach.
Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.
9
References [1] Ødegaard KM, Helseth E, Meling TR. Intraventricular meningiomas: a consecutive series of 22 patients and literature review. Neurosurg Rev 2013;36:57–64. [2] Wajima D, Iida J, Nishi N. Third ventricular meningioma–case report. Neurol Med Chir (Tokyo) 2011;51:75–8. [3] Avman N, Dinçer C. Meningiomas of the third ventricle. Acta Neurochir (Wien) 1978;42:217–24. [4] Cabezudo JM, Vaquero J, García-de-Sola R, et al. Meningioma of the anterior part of the third ventricle. Acta Neurochir (Wien) 1981;56:219–31. [5] Nakamura M, Roser F, Bundschuh O, et al. Intraventricular meningiomas: a review of 16 cases with reference to the literature. Surg Neurol 2003;59:491–503 [discussion 503–4]. [6] Karki P, Yonezawa H, Bohara M, et al. Third ventricular atypical meningioma which recurred with further malignant progression. Brain Tumor Pathol 2015;32:56–60. [7] Louis DN, Ohgaki H, Wiestler OD, et al. The 2007 WHO classification of tumours of the central nervous system. Acta Neuropathol 2007;114:97–109. [8] de la Sayette V, Rivaton F, Chapon F, et al. Meningioma of the third ventricle. Computed tomography and magnetic resonance imaging. Neuroradiology 1991;33:354–6. [9] Ito J, Kadekaru T, Hayano M, et al. Meningioma in the tela choroidea of the third ventricle: CT and angiographic correlations. Neuroradiology 1981;21:207–11. [10] Markwalder TM, Markwalder RV, Markwalder HM. Meningioma of the anterior part of the third ventricle. Case report. J Neurosurg 1979;50:233–5. [11] Rodrigues EA, Lawson AA. Meningioma of the third ventricle. Postgrad Med J 1982;58:498–500. [12] Rozario R, Adelman L, Prager RJ, et al. Meningiomas of the pineal region and third ventricle. Neurosurgery 1979;5:489–95. [13] Lozier AP, Bruce JN. Meningiomas of the velum interpositum: surgical considerations. Neurosurg Focus 2003;15:E11. [14] Song KS, Park SH, Cho BK, et al. Third ventricular chordoid meningioma in a child. J Neurosurg Pediatr 2008;2:269–72. [15] Wilson JL, Ellis TL, Mott RT. Chordoid meningioma of the third ventricle: a case report and review of the literature. Clin Neuropathol 2011;30:70–4. [16] Kasliwal MK, Srinivas M, Vaishya S, et al. Posterior third ventricular meningioma masquerading a pineal tumour. J Neurooncol 2006;78:103–4. [17] Lee YY, Lin SR, Horner FA. Third ventricle meningioma mimicking a colloid cyst in a child. AJR Am J Roentgenol 1979;132:669–71. [18] Renfro M, Delashaw JB, Peters K, et al. Anterior third ventricle meningioma in an adolescent: a case report. Neurosurgery 1992;31:746–50 [discussion 750]. [19] Pan J, Qi S, Lu Y, et al. Intraventricular craniopharyngioma: morphological analysis and outcome evaluation of 17 cases. Acta Neurochir (Wien) 2011;153:773–84. [20] Geng SM, Zhang JT, Zhang LW, et al. Optimal microsurgical treatment of dorsum sellae meningioma. Chin Med J (Engl) 2009;122:1857–61. [21] Hanieh A. Meningioma of the third ventricle. Childs Nerv Syst 1989;5:41–2. [22] Hori T, Kawamata T, Amano K, et al. Anterior interhemispheric approach for 100 tumors in and around the anterior third ventricle. Neurosurgery 2010;66:65–74. [23] Konovalov AN. Microsurgery of tumours of diencephalic region. Neurosurg Rev 1983;6:37–41. [24] Shiramizu H, Hori T, Matsuo S, et al. Anterior callosal section is useful for the removal of large tumors invading the dorsal part of the anterior third ventricle: operative technique and results. Neurosurg Rev 2013;36:467–75. [25] Strenger SW, Huang YP, Sachdev VP. Malignant meningioma within the third ventricle: a case report. Neurosurgery 1987;20:465–8. [26] Tekkök IH, Cag˘avi F, Güngen Y. FLAIR-positive MRI in an unenhancing meningioma of the third ventricle. Br J Neurosurg 2002;16:392–3. [27] Obrador S, Soto M, Gutierrez-Diaz JA. Surgical management of tumours of the pineal region. Acta Neurochir (Wien) 1976;34:159–71. [28] Mizowaki T, Nagashima T, Yamamoto K, et al. Optimized surgical approach to third ventricular choroid plexus papillomas of young children based on anatomical variations. World Neurosurg. 2014;82: 912.e15–9.
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Clinical Study
Third ventricular meningiomas Puxian Li a,b, Xingtao Diao a, Zhiyong Bi b, Shuyu Hao b, Xiaohui Ren b, Junting Zhang b,⇑, Jun Xing c a
Department of Neurosurgery, Laiwu Hospital, Taishan Medical University, Laiwu 271100, China Department of Neurosurgery, Beijing Tian Tan Hospital, Capital Medical University, Beijing 100050, China c Department of Medical, Laiwu Hospital, Taishan Medical University, Laiwu 271100, China b
a r t i c l e
i n f o
Article history: Received 9 February 2015 Accepted 1 May 2015 Available online xxxx Keywords: Clinical features Microsurgery Pathology Radiology Third ventricular meningioma Ventricular meningioma
a b s t r a c t We report 13 patients with third ventricular meningiomas (TVM) and discuss the clinical, radiological, pathological and surgical features, as well as follow-up of these tumors. TVM are rare intracranial tumors, and because of this, there are few reports in the literature. Of 11,600 intracranial meningiomas that were surgically treated and pathologically confirmed at Beijing Tian Tan Hospital over a period of 10 years (2003–2013), 13 TVM were selected for a retrospective review. We recorded the clinical, radiological, pathological, and surgical data and statistically analyzed the preoperative, postoperative and 6 month postoperative Karnofsky performance scale (KPS) scores. TVM represented 0.11% of intracranial meningiomas. Radiologically, TVM were divided into three groups: anterior (n = 3), posterior (n = 3), and entire third ventricle (n = 7). Three patients (23.1%) were misdiagnosed preoperatively. Total removal was achieved in 61.5% (8/13) of patients, and subtotal resection was achieved in 38.5% (5/13). Pathologically, the tumors were World Health Organization (WHO) Grade I in 11 patients (84.6%) and WHO Grade II in two (15.6%). There were no statistically significant differences in the preoperative, postoperative, or 6 month postoperative KPS scores (F = 0.814; p = 0.401). TVM without dural attachments are rare neoplasms that should be differentiated from choroid plexus papilloma, craniopharyngioma, and pineocytoma. Surgery is the optimal treatment and may result in a favorable prognosis, and understanding of the radiological subtype can help with the choice of surgical approach. Ó 2015 Elsevier Ltd. All rights reserved.
1. Introduction Intraventricular meningiomas are rare tumors, most of which are located in the lateral ventricle. They lack dural attachments and account for 0.5–5% of all intracranial meningiomas [1,2]. Third ventricular meningiomas (TVM) are extremely uncommon, representing only 0.1–0.18% of intracranial meningiomas [2–4]. An extensive review of the literature in 2003 found only 83 reported patients with TVM [5], and, to our knowledge, only seven further patients have been reported since 2003 in the English language literature. Therefore, a total of only 90 TVM have been reported to date. Most of these are from case reports or are sporadic cases in series of intraventricular meningiomas. Due to their deep location and proximity to crucial neurovascular structures, surgery for TVM is challenging. The morbidity and mortality rates were relatively high in early surgical reports. In 1978, Avman et al. [3] summarized 14 surgical TVM patients from the literature. Seven of these patients died after surgery, and five
⇑ Corresponding author. Tel.: +86 10 67098431; fax: +86 10 67051377. E-mail address: [email protected] (J. Zhang).
survived with severe neurological deficits. However, with advances in microsurgical techniques, perioperative equipment and postoperative intensive care, this situation has greatly improved. In 2014, Karki et al. [6] summarized nine patients with TVM. In their series, two patients died after surgery, but all others had good outcomes. Due to the rarity of the disease and the surgical challenges, further research is still needed to illuminate this rare entity. We retrospectively reviewed all TVM surgically treated and pathologically confirmed at Beijing Tian Tan Hospital over 10 years, from 2003–2013. Thirteen patients were identified, and the clinical, radiological, and pathological features, as well as surgical approaches and outcomes, were evaluated. To our knowledge, this is the largest single institution series of TVM.
2. Materials and methods A review of medical records identified 11,600 patients who underwent surgical treatment of pathologically confirmed intracranial meningiomas at Beijing Tian Tan Hospital during the study period. TVM were selected for analysis through a retrospective review of clinical, radiological, surgical, pathological and
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follow-up records. Prior written and informed consent was obtained from every patient, and the study was approved by the Ethics Review Board of Beijing Tian Tan Hospital. Clinical information was collected, including age and sex, symptoms and signs, the duration from symptom onset to admission, and preoperative diagnosis. The radiologic data included density on CT scans, intensity of T1- and T2-weighted enhancement on MRI, tumor location, tumor size, tumor shape, and the presence of hydrocephalus (based on MRI). The tumors were divided into three types according to location: anterior, posterior and entire third ventricle (using the massa intermedia as a boundary). Tumor size was defined as the maximum diameter on MRI. The surgical findings included the surgical approach, tumor color, tumor texture, tumor border, tumor blood supply, extent of tumor removal, blood loss during the operation, surgical time, surgical outcomes, and surgical complications. The extent of tumor removal was classified as total, subtotal or partial, based on the surgical records and postoperative MRI. The pathological type was determined according to the 2007 World Health Organization (WHO) classification of tumors of the central nervous system [7]. The follow-up data regarding complications, recurrences, treatment after discharge, and patient deaths were collected. Karnofsky performance scale (KPS) scores were also evaluated preoperatively, postoperatively and at 6 months after surgery. Statistical analyses were performed using SPSS software (version 17.0; IBM Corporation, Armonk, NY, USA). Statistical significance was defined as p < 0.05.
3. Results 3.1. Incidence and clinical features The incidence of ventricular meningiomas and TVM was 2.1% (240/11,600) and 0.11% (13/11,600) of all meningiomas, respectively. The clinical features of TVM are summarized in Table 1. Of the 13 TVM patients, there were seven males and six females. The age at hospital admission was 31.3 ± 18.3 years (mean ± standard deviation [SD]; range: 7–56). The duration from symptom onset to admission was a median of 12 months (range: 3 months to 5 years). In terms of the major symptoms and signs, eight patients presented with headaches, four with visual deficits, four with somnolence, three with ataxia, and three with limb weakness. Hearing loss, urinary incontinence, memory defect, and hormone abnormalities occurred in two patients each. Upgaze palsy, dysgraphia, amenorrhea, and diabetes insipidus occurred in one patient each. There were no patients with recurrent tumors or neurofibromatosis, and no patients underwent radiotherapy before hospital admission. Three patients (23.1%) were misdiagnosed preoperatively as having choroid plexus papilloma, craniopharyngioma, or pineocytoma (Fig. 1).
CT scans were available for seven patients. All tumors were hyperdense, and three had calcification. MRI examinations were performed for all patients. Seven tumors were isointense on T1and T2-weighted images. One tumor each was isointense on T1- and isohypointense on T2-weighted images, isointense on T1and hyper-hypointense on T2-weighted images, isohypointense on T1-weighted and hypointense on T2-weighted images, isointense on T1- and slightly hyperintense on T2-weighted images, slightly hypointense on T1- and isohyperintense on T2-weighted images and hypointense on T1- and T2-weighted images. MRI demonstrated homogenous enhancement in seven tumors, and heterogeneous enhancement in six. 3.3. Surgical findings and pathological types The surgical findings are summarized in Table 1, 3. Before surgery, one patient underwent placement of a ventriculoperitoneal shunt because of obstructive hydrocephalus. To remove the tumor, a right frontal craniotomy with a transcallosal transforniceal approach was performed in eight patients. A right frontal craniotomy with a transcallosal transventricular transchoroidal approach was performed in two patients, a right frontal craniotomy with a transcortical transventricular transchoroidal approach was performed in two, and an occipital transtentorial approach was used in one. Most of the tumors were gray–white in color (n = 9), three were gray–red, and one was pink. The tumor texture was tenacious in four, a mixture of firm and tenacious in three, soft in three, a mixture of soft and tenacious in one, and a mixture of firm, tenacious and soft in one patient. Seven tumors had a rich blood supply and six had a moderate blood supply. All tumors, except one, were well defined from the surrounding tissues. Total removal was achieved in eight (61.5%), and subtotal resection was achieved in five (38.5%) patients. The surgical duration was 7 ± 2.3 hours (mean ± SD; range: 4– 13). The mean blood loss during surgery was 500 ml (range: 200–2000). Eight patients had a drainage tube inserted, and all tubes were removed 1–3 days postoperatively. Regarding postoperative complications, electrolyte disturbances were found in six, hormone abnormalities in three, and subdural fluid accumulation in one patient. Diabetes insipidus, mutism, obstructive hydrocephalus, and intracranial infection occurred in two patients each. Two patients with obstructive hydrocephalus underwent a ventriculoperitoneal shunt placement after tumor removal. All complications were resolved before discharge, except in two patients who had hormonal abnormalities, one with diabetes insipidus who needed supplementary medication, and one with an intracranial infection who was discharged before the infection was controlled. The pathological subtypes are shown in Table 1. There were four fibrous, three lymphoplasmacyte-rich, and three transitional subtypes. Meningothelial, chordoid, and fibrous tumors with brain invasion were observed in one patient each (Fig. 5, 6). WHO Grade I tumors occurred in 11 patients (84.6%), and WHO Grade II in two (15.6%).
3.2. Radiological features 3.4. KPS and follow-up The radiological features are summarized in Table 1, 2. In terms of tumor location, there were three anterior, three posterior, and seven entire third ventricle type tumors (Fig. 2–4). Three tumors bulged into the bilateral lateral ventricles, two into the unilateral lateral ventricle, and two involved the septum pellucidum. In terms of the tumor shape, six were spherical, three were lobulated, and two were irregular. Dumbbell and cylindrical shapes were observed in one patient each. A total of nine patients had hydrocephalus, and nine had brain edema. The maximal tumor diameter was 5.1 ± 1.8 cm (mean ± SD; range: 2.3–8.2).
Data regarding the KPS are shown in Table 1. The median preoperative KPS was 80 (range: 70–100), and was unchanged postoperatively (median 80; range: 30–100). The median KPS 6 months after surgery was 90 (range: 0–100). There were no significant differences among the three groups on the test of repeated measures (F = 0.814; p = 0.401). All patients were followed up for 65.3 ± 42.9 months (mean ± SD; range: 3–129). Two patients had hormonal abnormalities, and one had diabetes insipidus, which resolved during the
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
Symptoms Patient Age (years), sex
Duration Preoperative (months) diagnosis
Tumor location Tumor in third ventricle size (cm)
Surgical approach
Extent of tumor removal
Pathological type
WHO KPS Grade Preop Postop 6 months postop
Transcallosal transventricular transchoroidal Transcallosal interforniceal Transcallosal interforniceal Occipital transtentorial Transcallosal interforniceal Transcallosal interforniceal Transcallosal transventricular transchoroidal Transcallosal interforniceal Transcortical transventricular transchoroidal Transcallosal interforniceal Transcortical transventricular transchoroidal Transcallosal interforniceal Transcallosal interforniceal
Subtotal
Transitional
I
70
90
100
Total
70
80
90
Total
Lymphoplasmacyte- I rich Meningothelial I
90
100
100
Subtotal
Fibrous
I
70
80
100
Total
80
90
90
Total
Lymphoplasmacyte- I rich Fibrous I
80
70
80
Subtotal
Transitional
I
80
80
100
Total
Fibrous
I
70
70
90
Total
Lymphoplasmacyte- I rich
80
70
90
Subtotal
80
70
70
Total
Fibrous, infiltrating II brain tissue Fibrous I
70
30
0
Subtotal
Transitional
I
100
100
100
Total
Chordoid
II
90
90
90
1
7, M
Headache, nausea, vomiting, gait ataxia, dysgraphia, 13 papilledema
Choroid plexus papilloma
Entire
7.4
2
28, F
12
Craniopharyngioma Entire
6.2
3
8, M
Headache, visual deterioration, memory deficit, amenorrhea, optic atrophy Headache, nausea, vomiting
2
Meningioma
Anterior
3
4
43, F
Headache, ataxia, upgaze palsy, left limb weakness
24
Meningioma
Posterior
5
5
30, M
12
Meningioma
Entire
5
6
46, F
Headache, visual deterioration, bilateral temporal hemianopsia, somnolence, diabetes insipidus Visual deterioration
3
Pineocytoma
Posterior
2.3
7
15, M
Headache, vomiting, right sided tinnitus, hearing loss 25
Meningioma
Entire
6.4
8
56, F
Meningioma
Entire
6.1
9
39, M
Right limb weakness, somnolence, urinary 13 incontinence Visual deterioration, bilateral temporal hemianopsia 60
Meningioma
Anterior
3.5
10
56, F
Somnolence
Meningioma
Posterior
5
11
12, M
Gait ataxia, left limb weakness, urinary incontinence 26
Meningioma
Entire
8.2
12
16, M
Headache
Meningioma
Entire
5.7
13
51, F
Headache, somnolence, memory defect, hearing loss 12
Meningioma
Anterior
3
6
3
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
Table 1 Clinical, radiological, and pathological features of 13 patients with TVM
KPS = Karnofsky performance scale, Postop = postoperative, Preop = preoperative, TVM = third ventricular meningioma, WHO = World Health Organization.
3
4
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Fig. 1. Patient 1, 2 and 6 were misdiagnosed with choroid plexus papilloma, craniopharyngioma, and pineocytoma, respectively. Patient 1: A lobular third ventricular tumor showed isointensity on (A axial) T1- and (B axial) T2-weighted MRI, and (C axial, D sagittal) homogeneous enhancement on the enhanced T1-weighted MRI; the tumor bulged into the right lateral ventricle. Patient 2: A dumbbell-shaped third ventricular tumor demonstrated (A axial) T1-weighted isointensity, (B axial) slight T2-weighted hyperintensity and (C axial, D sagittal, E coronal) homogeneous enhancement on the enhanced T1-weighted MRI. Patient 6: A spherical third ventricular lesion showed (A axial) high density and calcification on CT scan, and (B axial, D sagittal) iso- to hypointensity on the T1-weighted MRI, (C axial) hypointensity on the T2-weighted MRI, and (E axial) inhomogeneous enhancement on the enhanced T1-weighted MRI.
follow-up period. Three patients died during follow-up. One patient died of an intracranial infection 3 months after surgery, which was considered to be related to the surgery, one died of renal failure 2 years after surgery, and one died of gastric carcinoma 8 years after the meningioma surgery. Seven patients were able to continue with their normal studies or work, and three were able to live independently. No patient underwent radiotherapy or suffered a tumor recurrence. 4. Discussion TVM are a rare location of meningioma, and they can be easily misdiagnosed due to their atypical location and lack of dural attachment. Surgery for TVM is challenging due to the deep location and proximity to crucial neurovascular structures. Most of the reported patients are in case reports or are sporadic cases included in intraventricular meningioma series. From 2003–2013, 11,600 meningiomas were surgically treated in our hospital, 13 of which were confirmed to be TVM. To the best of our knowledge, this is the largest single institution series of TVM. 4.1. Incidence and origin of TVM The incidence of TVM is extremely low, with only 90 patients reported in the literature to date, including unspecified falcotentorial meningiomas [8–12]. The incidence of TVM is 0.1–0.18% of all intracranial meningiomas [2–4]. In the present series, only 13 TVM without dural attachment were found among the 11,600 intracranial meningiomas that were surgically treated and pathologically
confirmed at Beijing Tian tan Hospital over 10 years (2003– 2013), yielding an incidence of 0.11% of all meningiomas. It is known that most intracranial meningiomas occur in adults, with a female predominance. However, in our series, 31% (4/13) of TVM occurred in patients 6 16 years of age, with an almost equal male to female ratio. This finding is in accordance with most studies of TVM, which have reported a slightly higher incidence in males and the pediatric age group [3,9,12,13]. A comparison of previous studies and the present study of TVM is shown in Table 4. Because of a lack of symptoms early in the course of disease, or because of anticipated surgical challenges, some tumors can grow to a large size. The largest tumor in our series measured 8.2 cm, and most TVM were WHO Grade I (84.6%), with only two Grade II (15.4%). Among the WHO Grade II TVM, one was a chordoid meningioma, being only the third tumor of this type and location to have been reported [14,15]. Additionally, the fibrous meningioma of the third ventricle with brain invasion is the first to be reported, to our knowledge. TVM may originate from the choroid plexus, the tela choroidea of the velum interpositum, the tenia fornicis, or the connective tissue stroma of the pineal body [3,8–13,16]. Most authors suggest that the tela choroidea of the velum interpositum is the primary origin of TVM. During the initial stage of embryonic development, only one layer of the pia mater extends over the roof of the third ventricle, and when the corpus callosum extends posteriorly, it carries with it a layer of pia on its inferior surface, above the level of the choroid fissure. This overlies the original single pia layer, fusing with it to form the tela choroidea [9]. The velum interpositum is the potential space between the
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx Table 2 Radiological features of 13 patients with TVM Characteristics Location Anterior third ventricle Posterior third ventricle Entire third ventricle Bulging into left lateral ventricle Bulging into right lateral ventricle Bulging into bilateral lateral ventricles Bulging into septum pellucidum Shape of tumor Spherical Lobulated Irregular Dumbbell Cylindrical Hydrocephalus Yes No Brain edema Yes No Tumor size (cm) Mean ± SD Range CT scan Hyperdensity Calcification N/A T1-/T2-weighted MRI Isointense T1 and T2 Isointense T1, isohypointense T2 Isohypointense T1, isohyperintense T2 Isohypointense T1, hypointense T2 Isointense T1, light hyperintense T2 Slightly hypointense T1, isohyperintense T2 Hypointense T1 and T2 Enhancement Homogenous Heterogeneous
n (%) 3 3 7 1 1 3 2
(23.1) (23.1) (53.8) (7.7) (7.7) (23.1) (15.4)
6 3 2 1 1
(46.2) (23.1) (15.4) (7.7) (7.7)
9 (69.2) 4 (30.8) 9 (69.2) 4 (30.8) 5.1 ± 1.8 2.3–8.2 7 (53.8) 3 (23.1) 6 (46.2) 7 1 1 1 1 1 1
(53.8) (7.7) (7.7) (7.7) (7.7) (7.7) (7.7)
7 (53.8) 6 (46.2)
N/A = not available, SD = standard deviation, TVM = third ventricular meningioma.
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dorsal and ventral layers of the tela choroidea that contains the internal cerebral veins and medial posterior choroidal arteries. The velum interpositum, the two layers of the tela choroidea, and the body and crura of the fornices together form the roof of the third ventricle. The definition of the velum interpositum is often broadened to include the two layers of the tela choroidea, together with the velum interpositum proper [13]. In this study, we have used the broader term. Most TVM derive their blood supply from the medial posterior choroidal artery, but the lateral posterior choroidal artery, anterior choroidal artery, and even posterior pericallosal artery may contribute to the blood supply [8,9,12,13,15,17]. 4.2. Radiological type and its relationship to symptoms Previously, TVM have been divided into two radiological groups based on the involvement of the anterior and posterior parts of the third ventricle, and no line of demarcation was reported [4,8–13]. However, we found that some TVM occupied almost the entire third ventricle, so we divided the TVM into three groups: anterior, posterior, and entire (bounded by the massa intermedia). The anterior type TVM can compress the hypothalamus and optic tract, causing somnolence, memory deficits, hormonal abnormalities, diabetes insipidus or visual deficits. The posterior type may resemble pineocytomas and can compress the quadrigeminal plate, mesencephalon, cerebellum, or the medial and lateral geniculate bodies, leading to upgaze palsy (Parinaud’s syndrome), limb weakness, and gait ataxia, as well as visual or hearing deficits. The entire type can, therefore, have symptoms of both the anterior and posterior types. Tumor compression of the temporal lobe can cause language deficits, and compression of the fornix and hippocampus can cause memory loss. Mass effect and hydrocephalus can result in symptoms of increased intracranial pressure. Hydrocephalus alone can cause urinary incontinence as well as memory or visual deficits.
Fig. 2. Patient 9. Representative images of the anterior type third ventricular meningioma. A spherical third ventricular tumor showed mainly (A axial) high density on CT scan, and (B axial) iso- to hypointensity on T1-weighted MRI, (C axial) iso- to hyperintensity on T2-weighted MRI, and (D axial, E sagittal, F coronal) inhomogeneous enhancement on the enhanced MRI. (G axial) The postoperative T1-weighted MRI showed complete resection of the lesion. (H; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a lymphoplasmacyte-rich meningioma.
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
Fig. 3. Patient 4. Representative images of the posterior type third ventricular meningioma. On MRI, the spherical tumor was (A axial) isointense on T1-weighted images, (B axial) isointense on T2-weighted images, and (C axial, D sagittal, E coronal) homogenous enhancement on the enhanced T1-weighted MRI, with obvious hydrocephalus.
Fig. 4. Patient 11. Representative images of the entire type third ventricular meningioma. The tumor primarily demonstrated (A axial) isointensity on T1- and (B axial) T2weighted images, and (C axial, D sagittal, E coronal) heterogeneous enhancement on the enhanced T1-weighted MRI. The tumor filled the third ventricle and bulged into the bilateral lateral ventricles and septum pellucidum, with obvious hydrocephalus.
4.3. Differential diagnosis of TVM TVM lack dural attachments and are easily misdiagnosed. Choroid plexus papilloma, craniopharyngioma, astrocytoma, ependymoma, pituitary adenoma and colloid cysts should be differentiated from the anterior and entire types of TVM. Germ cell tumors and pineocytoma should be differentiated from posterior TVM. In our series, three patients (23.1%) were misdiagnosed preoperatively as having choroid plexus papilloma, craniopharyngioma, and pineocytoma. Choroid plexus papilloma generally occurs in children and has an irregular and cauliflower-like radiographic appearance. MRI usually demonstrates T1-weighted hypointensity, T2-weighted hyperintensity and obvious enhancement. Craniopharyngiomas can occur at any age, but most develop in children and adolescents. Craniopharyngioma usually presents with symptoms of hypopituitarism and hypothalamic damage, and calcification and cystic changes can be seen on imaging, but many ventricular craniopharyngiomas have no calcification or cystic changes [18]. Pan et al. [19] reported that 35.3% of ventricular craniopharyngiomas were completely solid and that 47.1% lacked calcification. Pineocytomas are located in the pineal region and usually develop in adults. Patients may have symptoms of Parinaud’s syndrome and arrest of sexual development. Calcification may be seen on CT scans, and these tumors usually demonstrate T1-weighted isointensity or hypointensity, T2-weighted hyperintensity and homogeneous enhancement on MRI. Despite advanced radiographic techniques, TVM are often misdiagnosed as other tumors, and confirmation of the diagnosis requires histopathology. 4.4. Selection of surgical approach for TVM and microsurgery The choice of surgical approach for TVM depends on the tumor location, adjacent structures (especially the deep venous systems), patient status and the surgeon’s preferences. For the anterior type of TVM, surgical approaches include the anterior transcortical transventricular transchoroidal/transforminal approach, the anterior interhemispheric transcallosal interforniceal approach, the anterior interhemispheric transcallosal transventricular tran-
Table 3 Surgical findings in 13 patients with TVM Characteristics Surgical approach Transcallosal interforniceal Transcallosal transventricular transchoroidal Transcortical transventricular transchoroidal Occipital transtentorial Tumor color Gray–white Gray–red Pink Tumor texture Tenacious Firm and tenacious Soft Soft and tenacious Firm, tenacious and soft Tumor blood supply Rich Moderate Tumor border Well defined Poorly defined Extent of resection Total Subtotal Operation time (hours) Mean ± SD Range Blood loss during operation (mL) Median Range Drainage tube insertion Yes No Postoperative complications Electrolyte disturbance Hormone abnormality Diabetes insipidus Mutism Obstructive hydrocephalus Intracranial infection Subdural fluid accumulation
n (%) 8 2 2 1
(61.5) (15.4) (15.4) (7.7)
9 (69.2) 3 (23.1) 1 (7.7) 4 3 3 2 1
(30.8) (23.1) (23.1) (15.4) (7.7)
7 (53.8) 6 (46.2) 12 (92.3) 1 (7.7) 8 (61.5) 5 (38.5) 7 ± 2.3 4–13 500 200–2000 8 (61.5) 5 (38.5) 6 3 2 2 2 2 1
(46.1) (23.1) (15.4) (15.4) (15.4) (15.4) (7.7)
SD = standard deviation, TVM = third ventricular meningioma.
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Fig. 5. Patient 13. Images of a third ventricular chordoid meningioma. The spherical tumor was located in the anterior part of the third ventricle and showed (A axial) high density on CT scan, (B axial) isointensity on T1- and (C axial) T2-weighted MRI, and (D axial, E sagittal, F coronal) homogeneous enhancement on the enhanced T1-weighted MRI. (G axial) Postoperative MRI revealed total resection of the tumor. (H; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a chordoid meningioma.
Fig. 6. Patient 10. Images of a third ventricular fibrous meningioma with brain invasion. The tumor demonstrated (A axial) isointensity on T1-weighted MRI, (B axial) iso- to hypointensity on T2-weighted MRI, and (C axial, D sagittal, E coronal) heterogeneous enhancement on the enhanced T1-weighted MRI. (F axial) The postoperative CT scan showed complete tumor resection and the insertion of a drainage tube into the third ventricle. (G; hematoxylin and eosin; magnification 100) Pathological examination showed that the tumor was a fibrous meningioma with brain invasion.
schoroidal/transforminal approach, the subfrontal, pterional or anterior interhemispheric translamina terminalis approaches, or the anterior callosal section combined with the anterior interhemispheric translamina terminalis approach [2–5,10,14,17,20–26]. For the posterior type of TVM, surgical approaches include the anterior
transcortical transventricular transchoroidal approach, the anterior interhemispheric transcallosal interforniceal approach, the anterior interhemispheric transcallosal transventricular transchoroidal approach, the posterior interhemispheric transcallosal approach, the infratentorial supracerebellar approach, and the occipital
Please cite this article in press as: Li P et al. Third ventricular meningiomas. J Clin Neurosci (2015), http://dx.doi.org/10.1016/j.jocn.2015.05.025
BI = brain invasion, F = female, M = male, N/A = not available, SD = standard deviation, TVM = third ventricular meningioma. a Sex information was not available for one patient.
Total (8); subtotal (5) Transcallosal interforniceal (8); transcallosal transventricular transchoroidal (2); transcortical transventricular transchoroidal (2); occipital transtentorial (1) 12 (3–60) 7:6 13 Present study
31.3 ± 18.3 (7–56)
N/A 6:2a 9 Karki et al.[6]
32.3 ± 24.8 (6–63)
7 (1–120) 11:6 17 Lozier et al.[13]
32.9 ± 17.6 (6–61)
N/A 11:11 22 Cabezudo et al.[4]
28.5 ± 17.9 (2–59)
Good (12); died 6 months postoperatively (1)
Good (7); died (2)
Meningothelial (1); atypical (1); chordoid (1); atypical-papillarymalignant (1); N/A (5) Fibrous (4); lymphoplasmacyte-rich (3); transitional (3); meningothelial with BI (1); chordoid with BI (1); fibrous with BI (1) Total (6); subtotal (1); debulking (1); N/A (1)
Total (13); subtotal (1); tumor not seen (1); N/A (2)
Fibrous (5); psammomatous (2); meningothelial (1); transitional (1); N/A (5) Fibrous (8); psammomatous (7); meningothelial (1); transitional (4); N/A (2) N/A Total (5); subtotal (1); N/A (8) 14 Avman et al.[2]
25.5 ± 17.0 (3–53)
7:7
24 (3–180)
Transventricular transforminal (3); anterior transcallosal (1); posterior transcallosal (2); N/A (8) Transventricular (11); anterior transcallosal (1); parieto-occipital (1); N/A (9) Infratentorial supracerebellar (4); occipital transtentorial (3); transcallosal (3); parieto-occipital (2); occipital (2); frontal (1); parietal (1); suboccipital (1) Transcortical transventricular (5); transcallosal (2); N/A (2)
Total (n = 13); subtotal (1); N/A (8)
Pathological type Extent of resection Surgical approach Symptom duration, median months (range) Sex, M:F Age, mean years ± SD (range) Patients, n Study
Table 4 Comparison of TVM features between previously reported studies and the present study
Survived with severe neurological deficits (5); died (7); N/A (2) Good (4); survived with neurological deficits (5); died (12); N/A (1) Good (4); survived with neurological deficits (8); died (2); N/A (3)
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Outcome
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transtentorial approach [3,9,12,13,27]. In our opinion, for the entire type of TVM, the anterior transcortical transventricular transchoroidal approach, the anterior interhemispheric transcallosal interforniceal approach, or the anterior interhemispheric transcallosal transventricular transchoroidal approach is suitable, as these tumors are usually large. A subfrontal approach, involving opening the frontal sinus, may increase the risk of infection, cosmetic abnormalities, extensive frontal lobe retraction, and olfactory bulb disruption [18]. The pterional approach provides limited exposure and is not suitable for large third ventricle tumors. Shiramizu et al. [24] believed that the anterior interhemispheric translamina terminalis approach could be used for anterior and inferior tumors of the third ventricle, but as the dorsal part of anterior third ventricular tumors is hidden from the anterior corpus callosum, requiring an anterior callosal section, the optimal indication for the combined approach is the treatment of tumors growing anteriorly from the line joining the anterior ridge of the foramen of Monro and the cerebral aqueduct. The transventricular approach is fit for TVM with dilation of the lateral ventricle, or a significant intraventricular component. The approach is generally through the right ventricle, as the right side is usually the non-dominant hemisphere, unless the tumor has an obvious and large projection into the left ventricle, in which case a left ventricular approach should be used. When a transventricular approach is used for a transcortical procedure, the cortical incision may lead to postoperative seizures and subdural fluid collections [2]. The transforminal approach is suitable for smaller tumors located in the anterior part of third ventricle, particularly if there is enlargement of the foramen of Monro. Also, the surgical field can be enlarged by dissecting the choroidal fissure, so that the field of view is increased [28]. The occipital transtentorial approach is appropriate for posterior type TVM that are centered in the quadrigeminal cistern and displace the deep venous system inferiorly. If the tumor originates from the ventral leaf of the tela choroidea and displaces the internal cerebral veins dorsally, the infratentorial supracerebellar approach is suitable. If the tumor originates from the dorsal leaf of the tela choroidea, displaces the internal cerebral veins ventrally, and does not extend posteriorly to the splenium of the corpus callosum, the posterior interhemispheric transcallosal approach can be selected [13]. In our series, the anterior interhemispheric transcallosal interforniceal approach or anterior interhemispheric transcallosal transventricular transchoroidal approach was performed in 77% (10/13) of patients. We prefer these two approaches for four reasons. First, the interhemispheric transcallosal approach reaches the third ventricle via natural anatomical spaces and without a cortical incision. Second, the interhemispheric transcallosal approach is suitable for almost all third ventricular tumors, especially for large tumors (most tumors in our series were large). Third, in our series, most patients had enlargement of the lateral ventricles due to hydrocephalus, allowing a transventricular approach. Lastly, our senior author is familiar with those two approaches. During surgery involving the interhemispheric transcallosal approach, long microsurgery instruments should be prepared, such as the long scissor, long bipolar forceps, and long aspirator. It is important to protect the cortical bridging veins and deep venous system, especially the internal cerebral veins, otherwise significant edema can result. If the internal cerebral veins are occluded, disastrous consequences may occur. The length of the corpus callosum incision should be limited to no more than 2.5 cm, or mutism or disconnection syndrome may result [20]. In our series, the corpus callosum incision was limited to 2 cm. In order to avoid injuring crucial adjacent structures, such as the hypothalamus and the deep venous system, the tumor should be removed in a piecemeal manner. Tumor tissue may occasionally need to be left behind,
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P. Li et al. / Journal of Clinical Neuroscience xxx (2015) xxx–xxx
particularly in situations where the tumor is closely adherent to a vital adjacent structure.
4.5. Management of TVM Although surgery for TVM is challenging, it is the optimal treatment for these benign tumors. Relatively positive results were achieved in our series of TVM patients following surgery. Total removal was achieved in 61.5% (8/13), and subtotal resection was performed in 38.5% (5/13) of patients. Only one patient died as a result of surgery, and there were no statistically significant differences between preoperative, postoperative, and 6 month KPS scores. At follow-up seven patients were able to continue with their normal study or work, three were living independently, and two died of other diseases. It is important to perform a detailed preoperative clinical and radiological evaluation in order to prepare patients for surgery and to decide on the optimal surgical approach. The management of postoperative complications is also important, including timely CT scans to rule out intracranial hematomas, close monitoring of postoperative water and electrolyte balance, monitoring and appropriate treatment of endocrine disturbances, and treatment of intracranial infections with antibiotics and drainage of lumbar or cerebrospinal fluid. Most patients with hydrocephalus improve after surgery, but if resolution does not occur, ventriculoperitoneal shunting can be performed. Gamma Knife (Elekta AB, Stockholm, Sweden) or photon radiation can be performed for the treatment of residual and recurrent TVM. Large field radiation is not suitable for these tumors because of their proximity to critical adjacent structures. Chemotherapy for these tumors is controversial, and no adjuvant treatment is needed for completely resected TVM.
5. Conclusion TVM without dural attachment are rare neoplasms, which should be differentiated from choroid plexus papilloma, craniopharyngioma, and pineocytoma. Surgery for TVM is full of challenges because of the deep location and crucial adjacent neurovascular structures. Nevertheless, surgery remains the optimal treatment and may result in a favorable prognosis. Definition of the radiological type and location can aid the choice of surgical approach.
Conflicts of Interest/Disclosures The authors declare that they have no financial or other conflicts of interest in relation to this research and its publication.
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