Displacement of mammillary bodies by craniopharyngiomas involving the third ventricle: surgical-MRI correlation and use in topographical diagnosis

Clinical article

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Object

Accurate diagnosis of the topographical relationships of craniopharyngiomas (CPs) involving the third ventricle and/or hypothalamus remains a challenging issue that critically influences the prediction of risks associated with their radical surgical removal. This study evaluates the diagnostic accuracy of MRI to define the precise topographical relationships between intraventricular CPs, the third ventricle, and the hypothalamus.

Methods

An extensive retrospective review of well-described CPs reported in the MRI era between 1990 and 2009 yielded 875 lesions largely or wholly involving the third ventricle. Craniopharyngiomas with midsagittal and coronal preoperative and postoperative MRI studies, in addition to detailed descriptions of clinical and surgical findings, were selected from this database (n = 130). The position of the CP and the morphological distortions caused by the tumor on the sella turcica, suprasellar cistern, optic chiasm, pituitary stalk, and third ventricle floor, including the infundibulum, tuber cinereum, and mammillary bodies (MBs), were analyzed on both preoperative and postoperative MRI studies. These changes were correlated with the definitive CP topography and type of third ventricle involvement by the lesion, as confirmed surgically.

Results

The mammillary body angle (MBA) is the angle formed by the intersection of a plane tangential to the base of the MBs and a plane parallel to the floor of the fourth ventricle in midsagittal MRI studies. Measurement of the MBA represented a reliable neuroradiological sign that could be used to discriminate the type of intraventricular involvement by the CP in 83% of cases in this series (n = 109). An acute MBA (< 60°) was indicative of a primary tuberal-intraventricular topography, whereas an obtuse MBA (> 90°) denoted a primary suprasellar CP position, causing either an invagination of the third ventricle (pseudointraventricular lesion) or its invasion (secondarily intraventricular lesion; p < 0.01). A multivariate model including a combination of 5 variables (the MBA, position of the hypothalamus, presence of hydrocephalus, psychiatric symptoms, and patient age) allowed an accurate definition of the CP topography preoperatively in 74%–90% of lesions, depending on the specific type of relationship between the tumor and third ventricle.

Conclusions

The type of mammillary body displacement caused by CPs represents a valuable clue for ascertaining the topographical relationships between these lesions and the third ventricle on preoperative MRI studies. The MBA provides a useful sign to preoperatively differentiate a primary intraventricular CP originating at the infundibulotuberal area from a primary suprasellar CP, which either invaginated or secondarily invaded the third ventricle.

Abbreviations used in this paper:CP = craniopharyngioma; MB = mammillary body; MBA = mammillary body angle; TVF = third ventricle floor.

Article Information

Address correspondence to: José María Pascual, M.D., Ph.D., Department of Neurosurgery, La Princesa University Hospital, C/Diego de León 62, 28006 Madrid, Spain. email: jmpasncj@hotmail.com.

Please include this information when citing this paper: published online March 29, 2013; DOI: 10.3171/2013.1.JNS111722.

© AANS, except where prohibited by US copyright law.

Headings

Figures

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    Coronal MR images demonstrating the relative anatomical positions between the hypothalamus and different topographical categories of intraventricular CPs. The upper row (A1, B1, and C1) shows the relative anatomical position of the hypothalamus (arrows) with respect to 3 different topographical categories of intraventricular CPs as observed on images obtained at the level of the third ventricle. The lower row images (A2, B2, and C2) show examples of similar CP–hypothalamus relationships in 3 intraventricular lesions corresponding to the same topographical categories, as observed in whole brain autopsy specimens. A1 and A2: Strictly intraventricular CP of the squamous-papillary type. Both hypothalami (arrows) are positioned adjacent to the inferior or lower-third tumor portion in both images. From Zülch KJ: Atlas of Gross Neurosurgical Pathology, Springer-Verlag, 1975, pp 155–160. Reprinted with kind permission of Springer Science+Business Media. B1 and B2: Not strictly intraventricular CP of the adamantinomatous type. Both hypothalami (arrows and arrowheads) are positioned around the middle-third portion (equator) of the tumor in both images. Notice the wide, tight attachment of the tumor to the floor and walls of the third ventricle with a layer of gliosis interposed between the outer capsule and the viable hypothalamus. From Choux M, Lena G: Craniopharyngioma, in Apuzzo MLJ (ed): Surgery of the Third Ventricle, ed 2. Williams & Wilkins, 1998, pp 1143–118. Reprinted with permission from Wolters Kluwer. C1 and C2: Pseudointraventricular CP. Both hypothalami (arrows) are positioned over the upper-third portion of the tumor in both images. Note the anatomically intact TVF pushed against the roof of the third ventricle by the mass, which is mimicking a true intraventricular position.

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    This illustration shows the MBA (red lines) as it is measured on a midsagittal section of the brain. The MBA is the angle formed by the intersection of the plane tangential to the base of the MBs with the plane tangential to the floor of the fourth ventricle (IV ventricle floor). In normal circumstances, the MBA in both adults and children has an acute value ranging between 50° and 70° (unpublished results).

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    Assessment of the MBs on midsagittal MR images, showing MRI-pathological correlation in the 4 major topographical categories of third ventricle CPs. Displacement of the MBs and their positional changes after surgical excision of a CP are shown on preoperative and postoperative midsagittal MRIs, respectively, for the 4 topographical categories of intraventricular CPs. Similar midsagittal macroscopic sections of a whole CP autopsy specimen are shown for each topography in the far right column (A3, B3, C3, and D3). A1–A3: Images showing an example of a strictly intraventricular type of CP. The MBs are observed to be squeezed beneath the lesion on the preoperative MR image (A1, arrow). An intact TVF, including atrophied MBs, is identifiable on the postoperative MR image after complete surgical removal of the lesion through a translamina terminalis approach (A2, arrow). These figures were published in Surg Neurol 33, Fukushima T, Hirakawa K, Kimura M, Tomonaga M: Intraventricular craniopharyngioma: its characteristics in magnetic resonance imaging and successful total removal, pp. 22–27, Copyright Elsevier (1990). A similar displacement of the MBs can be observed in the autopsy specimen corresponding to a strictly intraventricular CP (A3, arrow). From Vogel FS, Fuller GN, Bouldin TW: The nervous system, in Rubin E, Farber JL (eds): Pathology, ed 3. Lippincott-Raven Publishers, 1999, pp. 1442–1535. Reprinted with permission from Wolters Kluwer. B1–B3: Images showing an example of a not strictly intraventricular type of CP. The MBs are observed beneath the lesion on the preoperative MR image (B1, arrow). A breached or defective TVF is observed after complete surgical removal of the lesion through a combined translamina terminalis-transcallosal approach; the MBs are the only identifiable structures of the TVF on the postoperative midsagittal MR image (B2, arrow). The displaced MBs can be observed in the autopsy specimen corresponding to a not strictly intraventricular CP replacing the infundibulotuberal area (B3, arrow). Reprinted with permission from Fung K-M, Oklahoma Department of Pathology, University of Oklahoma Health Science Center, Oklahoma City (http://moon.ouhsc.edu/kfung/JTY1/NeuroTest/Q24-Ans.htm). C1–C3: Images showing an example of a pseudointraventricular type of CP. The MBs are observed being pushed upon by the lesion on a preoperative MR image (C1, arrow). The MBs are identifiable in a normal position on the postoperative MR image after complete surgical removal of the lesion through a basal approach (C2, arrow). These figures were published in Mehta V, Black PM: Craniopharyngioma in the adult, in Winn HR (ed): Youmans Neurological Surgery, ed 5. Saunders, pp 1207–1221, Copyright Elsevier (2004). A similar displacement of the MBs can be observed in the autopsy specimen corresponding to a pseudointraventricular CP (C3, arrow). This figure was published in Currie AR, Wyllie AH: The pituitary gland, in Symmers WStC (ed): Systemic Pathology, ed 2. Churchill Livingstone, Vol 4, pp 1863–1912, Copyright Elsevier (1978). D1–D3: Images showing an example of a secondarily intraventricular type of CP. The MBs are observed on preoperative MRI beneath a lesion originating within the sellar compartment (D1, arrow). The MBs are identifiable in a normal position on postoperative MRI after complete surgical removal of the lesion through a basal and translamina terminalis approach (D2, arrow). Note the wide defect in the TVF and the normal pituitary gland. Reproduced with permission from Türe et al.: J Neurosurg 87:706–715, 1997. The MBs can be observed in the autopsy specimen corresponding to a secondarily intraventricular CP (D3, arrow). From Zülch KJ: Atlas of Gross Neurosurgical Pathology, Springer-Verlag, 1975, pp 155–160. Reprinted with kind permission of Springer Science+Business Media.

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    Bar graphs showing changes in the MBA associated with specific CP topographies. A: Graph showing the ranges in the mammillary angle value (MBA) measured for each CP's topographical category on preoperative midsagittal MR images. Note the opposite distribution of values between the pseudointraventricular topography, in which 90% of lesions showed MBA values greater than 90°, and the strict and not strict intraventricular topographies, both showing MBAs of less than 90° in all cases (p < 0.001, Pearson chi-square test). On average, the not strictly intraventricular category was associated with lower, or more acute, MBA values than the strictly intraventricular category. B: Graph demonstrating ranges in the MBA value measured postoperatively for each CP topography. Note the marked change in the ranges of MBA values shown postoperatively in each topographical category by comparing the distribution of bars between graphs A and B. Most of the obtuse (> 90°) MBA values measured preoperatively in the pseudointraventricular category have an acute value between 31° and 90° postoperatively, a change indicating a recovery in the position of the MBs after surgical removal of the tumor. In a similar way, the hyperacute (< 30°) MBA values measured preoperatively in the strict and not strict intraventricular categories are in the range of 31°–90° after surgical excision, indicating normalization in the anatomical position of the MBs. C: Graph showing types of changes in the MBA observed postoperatively for each CP topographical category. An acute type of change in the value of the MBA (from an MBA > 90° to one < 90°) characterizes the pseudointraventricular topography. The strict and not strict intraventricular categories show a similar relative proportion of obtuse changes (from a hyperacute MBA value to a less acute one) and no significant changes in the MBA (postoperative change < 10° in the MBA). However, the absolute change in the MBA was higher in the not strictly intraventricular category than in the strictly intraventricular category (p < 0.001, Pearson chi-square test). The secondarily intraventricular category showed the highest variability in the type of MBA change, with a similar number of cases undergoing an acute or obtuse modification of this value. No. = number of cases.

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    Data on MBA for discrimination of topographical categories of intraventricular CPs. A: Table showing mean (°), median (°), and SEM of the MBA values in each CP topography. B: Box plot comparing the preoperative MBA measured for each CP topography. A marked higher clustering of MBA values was measured in the pseudointraventricular topography. The infundibulotuberal, or not strictly intraventricular, category displayed the lowest mean and median MBA values, in accordance with the expansion of these lesions within the TVF causing the greatest backward displacement of the MBs. The highest dispersion of MBA values is observed in the secondarily intraventricular topography, in agreement with the multiplicity of points of origin of the lesion along the pituitary-hypothalamus axis. C: Table showing sensitivity and specificity values of the preoperative MBA calculated by regression logistic analysis for every pair of CP topographical categories. D: Table listing global classification results using the MBA. The absolute number of CPs correctly assigned to their topographical category and the rates of correct topographical diagnosis obtained with the use of the MBA are displayed. The pseudointraventricular topography is correctly discriminated in 94% of cases and the not strictly intraventricular topography in 67.5%. Not Strictly IV = not strictly intraventricular topography; Pseudo IV = pseudointraventricular topography; Secondary IV = secondarily intraventricular topography; Strictly IV = strictly intraventricular topography.

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    Multivariate model for discrimination of topographical categories of intraventricular CPs. A: Vectorial graph showing component loadings analysis after optimal scaling of neuroradiological variables. The neuroradiological (MRI) categorical variables considered in the study were transformed into ordinal variables by an optimal scaling process and each of the variables is represented in the graphic as a vector projected into a 2D space. The ordinal scaling is displayed for the topographical category vector (red), the mammillary angle (blue), and the hypothalamus position (brown). The angle between 2 pair of vectors is proportional to the degree of correlation of the variables represented by such vectors. The absolute values of the correlations between all the transformed neuroradiological variables after optimal scaling and the CP topography are shown in the list below the vectorial graphic. The 2 variables showing the highest negative correlations with the CP topographical categories considered were the preoperative MBA value (blue vector) and the relative anatomical position of the hypothalamus (brown vector). This negative correlation indicates that a higher MBA value and an upper hypothalamus position (values at the end of their respective vectors) are correlated with the pseudointraventricular topography (the first position in the CP topography vector). In contrast, a lower MBA value and a lower hypothalamus position are correlated with the strictly intraventricular category. B: Scatter plot representing the topographical differentiation of the CPs in a 2D space defined by the discriminant coefficients of 5 variables selected in a stepwise discriminant analysis. Topographical categories were optimally discriminated with a model of 5 variables selected from the pool of variables analyzed in the study through a process of stepwise discriminant analysis. These 5 variables were the preoperative MBA, the relative position of the hypothalamus, the presence of hydrocephalus, the presence of psychiatric symptoms, and patient age. The canonical discriminant coefficients calculated for these variables are shown below the figure. The groups of pseudointraventricular and secondarily intraventricular CPs can be discriminated from the strictly and not strictly intraventricular topographies on dimension 1 (factor 1) by their higher (more positive) MBA values and the upper (more positive) hypothalamus level. The strictly intraventricular category is best discriminated from the not strictly intraventricular topography on dimension 2 (factor 2) by a higher rate of psychiatric symptoms (more positive), hydrocephalus, and an older patient age.

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    Illustrations showing changes in the MBA caused by progression of intraventricular CPs, including differential effects of specific CP topographies. a1–a4: Midsagittal brain section showing the backward displacement of the MBs caused by the growth of an intraventricular CP that originated at the infundibulotuberal area of the TVF (infundibulotuberal or not strictly intraventricular CP). The value of the MBA (red lines) undergoes a progressive decrease (more acute MBA) as the tumor mass expands in the third ventricle until the MBs become compressed against the midbrain. b1–b4: Similar illustrations showing the opposite change in the MBA caused by a primary suprasellar lesion that pushes the TVF upward, mimicking a third ventricle position (pseudointraventricular CP). The value of the MBA (red lines) undergoes a progressive increase (more obtuse MBA) as the tumor mass folds inwards into the TVF until the MBs become compressed against the fornices and roof of the third ventricle.

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