Neuroradiology

, Volume 54, Issue 12, pp 1341–1346

Bochdalek’s flower basket: applied neuroimaging morphometry and variants of choroid plexus in the cerebellopontine angles

Authors

  • Avril Horsburgh
    • Department of RadiologyAddenbrooke’s Hospital
  • Ramez W. Kirollos
    • Department of NeurosurgeryAddenbrooke’s Hospital
    • Department of RadiologyAddenbrooke’s Hospital
    • Department of RadiologyUniversity of Cambridge
    • University Department of Radiology, Addenbrooke’s HospitalUniversity of Cambridge School of Clinical Medicine
Diagnostic Neuroradiology

DOI: 10.1007/s00234-012-1065-1

Cite this article as:
Horsburgh, A., Kirollos, R.W. & Massoud, T.F. Neuroradiology (2012) 54: 1341. doi:10.1007/s00234-012-1065-1
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Abstract

Introduction

Protrusions of fourth ventricular choroid plexus through the foramina of Luschka are called ‘Bochdalek’s flower basket’ (BochFB). The bulbous terminal expansions (cornucopiae) extend into the cerebellopontine angle (CPA) cisterns. We studied and reviewed the normal imaging anatomy, morphometry and anatomical variants of BochFB.

Methods

We retrospectively analysed normal brain imaging findings on axial pre- and post-contrast CT scans and enhanced axial T1-weighted MRIs of 200 patients. We assessed BochFB for: (a) calcification, (b) lateral extension, (c) enhancement pattern, (d) cornucopiae shape, (e) symmetry and (f) proximity to tortuous vertebral arteries and morphometry of cornucopiae size and length of BochFB limbs.

Results

BochFB calcification was found in 38 % of patients aged over 51 years. Lateral extension of BochFB into the CPA cistern was prominent in 75 % on CT and 96 % on MRI. The mean length of these extensions was 23.6 mm. BochFB enhanced strongly in 47 % on CT and 66 % on MRI. The BochFB cornucopiae were bulbous in 51 % on CT and 54 % on MRI. The mean width of bulbous cornucopiae was 3.5 mm. Bilateral BochFB symmetry was found in 71 % on CT and 80 % on MRI. Six to 8 % of tortuous left vertebral arteries were close to BochFB.

Conclusion

The cornucopiae are particularly well demonstrated on post-contrast MRI. However several sources of error in image interpretation may arise when imaging the normal BochFB on routine head CT and MRI. Difficulties in analysis arise especially on CT because of physiologic calcification, asymmetry, and the bulbous cornucopiae being mistaken for aneurysms.

Keywords

AnatomyBochdalekChoroid plexusCerebellopontine angleAnterior inferior cerebellar artery

Introduction

The lateral limbs of the choroid plexus of the fourth ventricle are horizontally positioned in the lateral recesses of the fourth ventricle [1, 2]. The protrusions of the choroid plexus from the lateral foramina of Luschka are called Bochdalek’s flower basket (Blumenkőrbchen, BochFB) [3], the bulbous terminal expansions (cornucopiae) of which extend into the cerebellopontine angle (CPA) cisterns [4, 5] (Fig. 1). Sources of error in image interpretation may arise when BochFB is imaged on routine head CT and MRI, on account of normal calcification, asymmetry, and enhancing bulbous cornucopiae being misinterpreted for aneurysms or, more rarely, for tumors, e.g. choroid plexus papilloma at the CPA [6].
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Fig. 1

Protrusions of the fourth ventricular choroid plexus through the foramina of Luschka are called ‘Bochdalek’s flower basket’ (BochFB). a Diagrammatic representation of BochFb (slice f) in the axial plane as it forms part of the choroid plexus of the fourth ventricle. Slices ag represent schematics of axial cross-sectional imaging through the fourth ventricle when performed parallel to the orbital plane. Slices dg are those including and depicting the choroid plexus, the structure of which is described in detail in the ‘Discussion’ section. Reproduced with permission of reference number [4]. b Axial post-contrast T1WI MRI showing the bulbous terminal expansions (cornucopiae) of BochFB extending into the CPA cisterns (left side, arrow)

Precise appreciation of normal anatomical relationships between brain structures, intracranial vessels and subarachnoid spaces would allow optimal neuroradiological diagnosis, neurosurgical planning, minimize procedure related complications and optimize surgical and patient outcomes. Greater awareness and knowledge of the normal anatomy of this region in particular would be valuable for neuroradiologists in their aim to reduce inaccuracy and misdiagnosis, and for neurosurgeons, where, for instance, this would be of significant use in operations involving the CPA cistern and in those in which the foramen of Luschka is used as a corridor to reach the interior and floor of the fourth ventricle [7]. Further applications in neuroendoscopy include, for example, minimally invasive placement of auditory brainstem implants to directly stimulate the cochlear nuclei in patients deafened by loss of the vestibulocochlear nerves [8]. Endoscopic access to the dorsal cochlear nucleus in the lateral recess of the fourth ventricle entails tracking the choroid plexus of BochFB under direct vision through foramen of Luschka and into the lateral recess of the fourth ventricle [9]. Together with a thorough understanding of anatomical details reflected in textbooks and atlases of anatomy, the combined use of sophisticated high-resolution three-dimensional neuroimaging techniques is the very basis of successful preoperative planning for open and neuroendoscopic surgery.

This is the first investigation of the normal imaging anatomy and morphometry of the portions of the choroid plexus of the fourth ventricle that extend into the CPA cisterns (the lateral horizontal segments [1]), as seen on cross-sectional CT and MRI. We classify the anatomical variants of BochFB and review the applied vascular anatomy relevant to these findings.

Methods

All imaging was performed during routine neuroadiological work-up of patients based on clinical indications; no prospective imaging of normal volunteers was performed in this study. As such, according to guidelines of the revised Declaration of Helsinki, this study reported the retrospective analysis of anonymized data (images) obtained from ‘routine sources’ where consent of individual patients and ethical approval for research analysis was therefore not considered necessary [10, 11].

First we retrospectively reviewed standard pre- and post-contrast head CT scans on 100 patients obtained over a 1-year period and who demonstrated normal imaging findings. All axial contiguous slices through the posterior fossa were 4.5-mm thick and were obtained using a Siemens SOMATOM Sensation® 16 CT scanner. Contrast enhanced images were obtained after intravenous injection of 50 ml of non-ionic contrast medium (iopamidol, 300 mg iodine per ml). Two radiologists retrospectively analysed all anonymized images of the entire brain to confirm the absence of pathology, and subsequently concentrated on images through the posterior fossa to study the anatomy of BochFB. We reviewed, and by consensus agreed upon, the findings on the images for the following BochFB features: (a) calcification; (b) lateral extension: ‘full bouquet’, ‘posy’ or ‘single stem’; (c) enhancement pattern: prominent, moderate, faint or speckled; (d) cornucopiae shape: bulbous, flat or both; (e) symmetry and (f) proximity to tortuous vertebral arteries.

Next, we retrospectively reviewed standard 1.5T brain MRI post-contrast T1 weighted images of 100 different patients obtained over the same 1-year period and also with normal imaging findings. We used a 1.5T magnet (Signa HDx, GE Healthcare, Waukesha, WI) and a standard head coil with eight elements (8 HR Brain; GE Healthcare). Patients were scanned with a standard imaging protocol: TR 540, TE 19, FOV 18 cm, matrix 320 × 224, slice thickness 2 mm and slice gap 2.5 mm. Contrast enhanced images were obtained after intravenous injection of 5 ml of Gadovist® (gadobutrol, 1 mmol/ml). Again, the same two radiologists retrospectively analysed all anonymized images of the entire brain to confirm the absence of pathology, and subsequently concentrated on images through the posterior fossa to study and agree by consensus on the anatomy and morphometry of BochFB, as described above for the CT images. Additionally, we used electronic callipers on a PACS review workstation to measure the mean width of cornucopiae, and the mean length of each choroid plexus limb from the midline outwards on MR images of BochFB.

Results

In the CT group, patients were a mean age of 60 year (46 % female and 54 % male). BochFB calcification was present in 38 % (heavy in 6 [Fig. 2a], moderate in 26, and faint in 6) of patients above the age 51 year. Lateral extension of BochFB into the CPA cistern was prominent, similar to a full bouquet (in 75 [Fig. 2a]), moderate (a posy in 18) or a slender extension (single stem in 3). The enhancement pattern of BochFB was prominent in 47 (Fig. 2b), moderate in 12, faint in 15 or very faint in 26. The shape of BochFB cornucopiae was bulbous in 51, flat in 30 or both bulbous and flat in 19. Bilateral BochFB symmetry was found in 71 % of patients, with mild asymmetry in 25 %, and 4 % had one side missing or invisible on CT (Fig. 2c). Six vertebral arteries were close to the left aspect of BochFB, and two were on the right.
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Fig. 2

Axial cross-sectional imaging through the posterior fossa demonstrating examples of BochFB morphology and imaging characteristics. a Unenhanced CT showing a ‘heavily calcified full bouquet’. b Post-contrast CT showing lateral extension of BochFB into the CPA cistern with ‘strong enhancement’. c Post-contrast CT showing an ‘asymmetric’ BochFB with enhancement only on the right (arrow). d Post-contrast T1WI MRI showing subtle enhancement of a slender BochFB classified as a ‘single stem’. e Post-contrast T1WI MRI showing a BochFB with ‘bulbous cornucopiae’

The mean age in the MRI group was 58 years (46 % female and 54 % male). Lateral extension of BochFB into the CPA cistern was prominent (full bouquet in 96), posy in 2, or single stem in 2 (Fig. 2d). The enhancement pattern of BochFB was prominent in 66, or faint in 44. The shape of BochFB cornucopiae was bulbous in 54 (Fig. 2e), flat in 40 or both in 6. Bilateral BochFB symmetry was found in 80 % of patients. Eight vertebral arteries were close to BochFB on the left (Fig. 3) and 1 on the right. The mean antero-posterior width of bulbous cornucopiae was 3.5 mm, and the mean length of the lateral horizontal segments of the fourth ventricular choroid plexus (measured from the midline), including the limbs of BochFB when demonstrating a full bouquet, was 23.6 mm.
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Fig. 3

Axial post-contrast T1WI MRI showing the left vertebral artery in close proximity to the cornucopia of the left aspect of BochFB (arrow)

Discussion

Difficulties and errors in image interpretation of BochFB may arise on routine diagnostic cross-sectional imaging of the brain, especially head CT scans, on account of normal calcification, asymmetry and bulbous ends of BochFB being misinterpreted as aneurysms or tumors. We therefore set out in this study to classify the appearances of BochFB and establish the frequency of its visualization, calcification, asymmetry, extent and proximity to arteries of the posterior fossa.

Choroid plexus relationship to foramina of Luschka

The choroid plexus of the fourth ventricle begins to appear as an invagination of mesenchymal-derived epithelial tissue pushing into the neural tube soon after it closes [12]. Thus, the choroid plexus rests along the posterior inferior wall of the fourth ventricle. It is a paired structure with two components [1]. A paramedian ‘medial’ limb parallels the long axis of the brainstem and lies against the lateral surface of the vermis. It joins a horizontal ‘lateral’ limb which lies in the lateral recess of the fourth ventricle. The lateral recesses are narrow, curved pouches formed by the union of the roof and the floor of the fourth ventricle [13]. They extend laterally below the cerebellar peduncles, which open through the foramina of Luschka into the CPA cisterns. The lateral recesses were discovered by Bochdalek in 1849 and mistakenly thought to be blind extensions of the fourth ventricle, but they were later correctly revealed as channels communicating with the subarachnoid space by Luschka in 1855 [14]. Thus, the foramina of Luschka are the site of exit of the lateral limbs of the fourth ventricular choroid plexus as well as free communication with the subarachnoid space. Sharifi et al. divided each foramen of Luschka into two compartments, one compartment was the real opening or the patent part and the other compartment was the choroidal part where choroid plexus extends into the CPA cistern [15]. It has been shown previously that the choroid plexus extending from the left and right foramina of Luschka have a mean height of 5.31 and 5.4 mm, and a width of 6.49 and 6 mm, respectively [15].

Bochdalek’s flower basket

Vincenz Alexander Bochdalek (1801–1883) was a skilful anatomist and pathologist who studied and worked at Charles-Ferdinand University in Prague from the 1820s to the early 1870s [3]. His legacy in anatomy is considerable and several eponymous anatomical structures are associated with him. The protrusions of the choroid plexus from the lateral foramina of Luschka are called Bochdalek’s flower basket. This originates as extensions of the horizontal limbs of the choroid plexus within the lateral recesses of the fourth ventricle. Upon exiting foramina of Luschka, they terminate in bulbous expansions called cornucopiae lying within the CPA cisterns. BochFB protrudes from the foramen of Luschka behind the glossopharyngeal and vagus nerves [13], and each cornucopia marks the anterior surface of the ipsilateral cerebellar hemisphere at the level of the seventh and eighth cranial nerve roots [5]. Each limb of BochFB (along with the cerebellar flocculus) extends laterally above the lower limb of the cerebellopontine fissure [15]. The cerebellopontine fissure is a V-shaped fissure located where the cerebellum wraps around the pons and middle cerebellar peduncle. This fissure consists of two limbs, inferior and superior limbs and the CPA is situated between the superior and inferior limbs of this fissure [13].

Calcification and symmetry of the flower basket

Adequate visualization of the choroid plexus of the fourth ventricle on cross-sectional imaging depends on the dose of contrast medium used, the technical quality of the scans, the scan angle and the use of overlapping scan sections [4]. Nowadays this structure is seen in most patients on routine CT and MRI scans. Our CT cases were viewed at routine window levels and widths. With high window levels and low window widths, additional fine punctate calcification of the choroid plexus can be identified on CT [16].

Choroid calcification in the roof of the fourth ventricle is frequently found at autopsy [17]. We demonstrated that 38 % of BochFB was sufficiently calcified to be visible on unenhanced CT scans. This is unlike the findings of Modic et al. who did not visualize any physiologic calcification in the choroid plexus of the fourth ventricle on 1,000 CT scans performed on patients of all ages examined on previous generation scanners in 1980 [16]. Modic et al. also found the incidence of calcification of the choroid plexus of the lateral ventricle to be 0.5 % in the first decade and 86 % in the eighth decade [16]. Interestingly the incidence of physiologic glomus calcification in the fifth decade of life was found to rise steeply to 75 % from 35 % in the prior decade.

In our study, higher-resolution MRI was able to demonstrate greater symmetry (80 %) of bilateral limbs of BochFB than seen on CT (71 %). Bradac et al. found symmetry of the two sides of the fourth ventricular choroid plexus in 96.5 % of 57 brain dissections [18]. We found that the BochFB limbs protruded by a mean length of 23.6 mm into the CPA cisterns.

Avoidance of diagnostic misinterpretation by understanding relationships to adjacent arteries

Understanding the close relations between several arteries in the CPA cistern, the choroid plexus of BochFB and foramen of Luschka is of critical importance to accurate interpretation of cross-sectional images in this region. When a small discrete rounded hyperdense mass, seen particularly on either pre- or post-contrast CT scans, is noted in the CPA cistern in the vicinity of foramen of Luschka, it can raise the diagnostic dilemma of whether this represents a conspicuous asymmetrically enlarged cornucopia, an aneurysm of the anterior or posterior inferior cerebellar arteries (AICA, PICA), or an enlarged/tortuous vertebral artery. An example of such a case is illustrated in Fig. 4. Moreover, correct interpretation of the imaging findings in the midst of these various anatomical relations is crucial for neurosurgical and neuroendoscopic procedures in which the foramen of Luschka is used to access the fourth ventricle.
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Fig. 4

a Axial pre-contrast CT showing a small discrete calcified mass in the right CPA initially thought to possibly represent an aneurysm (white arrow). b To clarify this, the patient went on to have a 3D TOF MRA, the axial MIP images of which did not reveal an aneurysm, demonstrating it instead to be a prominent bulbous cornucopia of BochFB (white arrow)

We therefore carefully studied the frequency with which the vertebral arteries lie close to BochFB within the CPA cisterns. We did not investigate this similar relation for either AICA or PICA because the proximity of these arteries to foramen of Luschka is already well documented in the literature [1, 15], and their normal (non-aneurysmal) small calibre would most unlikely create any diagnostic misinterpretation with cornucopiae of BochFB. However, aneurysms of these arteries might do, and further exploration of this might require the analysis of cross-sectional imaging appearances in a separate population of patients harbouring aneurysms of these two arteries. On the other hand, a tortuous vertebral artery, which is normally larger in size than AICA or PICA, may occasionally occupy the CPA and further add to the complexity of the region, or may compress or block the entrance of the foramen of Luschka [15]. Tortuousity of the normal vertebral arteries was therefore amenable to study on the scans of our patients with normal findings.

In our CT group, six vertebral arteries were close to the left aspect of BochFB, and two were on the right. In the MRI group, eight vertebral arteries were close to BochFB on the left, and one was on the right. By comparison, Sharifi et al. found that in 10 of 40 cases at post-mortem (arteries injected with coloured gelatine) the left vertebral had a tortuous course toward the left CPA and foramen of Luschka, but no such tortuous right vertebral artery was found in their material [15].

The two main arteries that supply the cerebellum, AICA and PICA, originating from the basilar and vertebral arteries, have very close relations with the foramen of Luschka and BochFB, as reported by Sharifi et al. [15], and worthy of note here. AICA is the main source of blood supply to the lateral horizontal segment of the fourth ventricular choroid plexus and BochFB [1]. It runs near the foramen of Luschka in the lateral part of the cerebellomedullary fissure and sometimes sends some branches into the foramen of Luschka, before turning away from the fissure. Sharifi et al. found that the mean closest distance between AICA and foramen of Luschka is 3.90 and 3.89 mm on the left and right sides, respectively [15]. Overall 10 AICA’s on the left and 6 on the right (out of 40 specimens) were within 1 mm of foramen of Luschka. PICA runs around the tonsil in the medial part of the cerebellomedullary fissure and bifurcates into the vermian and hemispheric branches [15]. Sharifi et al. found that the average distance between the foramen of Luschka and PICA was 7.08 and 5.81 mm for the left and the right sides, respectively [15]. Seven PICAs on the left and 12 on the right also were within 1 mm of foramen of Luschka. Variation in size of AICA usually is in inverse proportion to the size of PICA [19].

Conclusion

Several sources of error in image interpretation may arise when imaging the normal BochFB on routine head CT and MRI. The cornucopiae are particularly well demonstrated on post-contrast MRI. Difficulties in diagnosis arise especially on CT because of physiologic calcification, asymmetry and the bulbous cornucopiae being mistaken for aneurysms or tortuous vertebral arteries.

Acknowledgment

TFM was supported by the NIHR Cambridge Biomedical Research Center.

Conflict of interest

We declare that we have no conflict of interest.

Copyright information

© Springer-Verlag 2012