INTRODUCTION

Outward indentation of the choroid plexus from the foramen of Luschka, also known as Boc FB, was first found by the Czech anatomist Vincent Alexander Bochdalek (1801–1883), who also described the Bochdalek hernia [16]. Although this finding is relatively common, it does not take place in radiological reports and is often overlooked [11]. So far, studies on this subject are based on examination with magnetic resonance imaging (MRI). The morphology of Boc FBC is emphasized in MRI studies. However, Boc FB can also be calcified like the choroid plexus. While MRI shows anatomical structure very well, calcifications are technically the weak point for this method. Therefore, our study was based on non-contrast computed tomography (CT) since it is the gold standard for calcification assessment. To the best of our knowledge, our study is the first CT study on this subject and there is no detailed information in English literature about Boc FB calcifications (Boc FBC). It is important to know the features of calcifications along with the part of the choroid plexus in this region. Since calcifications don’t occur in all of the parts of Boc FB, it may be confused with the surrounding non-calcified fragment, haemorrhages and with cerebellopontine angle masses because this entity is not well-known by some radiologists [3, 11, 22]. Although textbooks express that the distinction between haemorrhage and calcifications can be made with coarse morphology and measurements of Hounsfield units (HUs), there are many pitfalls. Based on calcium amount and region of interest cursor, the HU values change [12]. Since vascular calcifications and Boc FBCs are seen in the same age group, when the vessel is tortuous, the Boc FBCs and vascular locations overlap and can be confused. Therefore, calcifications of the vertebral and basilar arteries are part of the differential diagnosis of Boc FBC due not only to the age group but also to the location [3, 11, 12, 18, 22].

When we mention choroid plexus calcifications, usually calcifications of the lateral ventricle or rarely the plexus part of the third ventricle come to mind. However, the choroid plexus extends to the fourth ventricle and can reach variationally cerebello-pontine cistern via foramen of Luschka. In other words, calcifications originating from the choroid plexus can be seen not only in the lateral ventricle and the third ventricle but also on the wall of the fourth ventricle as well as out of the ventricles, such as Boc FBC [15, 22].

Some areas such as the basal ganglia, the pineal/habenular glands, other parts of choroid plexus and vascular structures tend to calcify with ageing [25]. As far as we know, the relationship between these calcifications and Boc FBCs has been also compared for the first time in our study.

The study aims to help prevent erroneous reporting by identifying the morphology of a not well-known variational anatomical structure’s calcification ‘Boc FBC’.

MATERIALS AND METHODS

This study was approved by Muğla Sıtkı Koçman University Human Research Ethics Committee with the document number: 200027/2020. The design and conduct of the study were in accordance with the general principles set out in the Declaration of Helsinki. The patients who underwent CT scans between January 2016 and June 2021 for various indications were retrospectively evaluated in terms of Boc FBC and accompanying intracranial calcifications. All of the images were obtained from picture archiving communication systems.

Power analysis was performed with a G-power test. An appropriate sample size was calculated at 111 for creating 0.95 (actual power: 0.9503016, critical t: 1.6589535). Power (1-b prob) based on 0.05 alfa error prob. The number of patients in our study was sufficient. Two hundred sixty-four CTs of healthy patients (50.0 ± ± 24.78/0–92 years old [mean ± standard deviation/range]) as 120 (45.5%) females and 144 (54.5%) males were included in the study. We excluded 34 patients from the study because of the following medical reasons: 23 patients had different major pathologies (mass, infarct, aneurysm, infection, bleeding), 9 had history of operation, 2 had motion artifacts.

Cranial CT scans were performed with a 256-slice multi-detector CT scanner (Somatom, Siemens Healthcare, Erlangen, Germany). The protocol used for cranial CT is as follow: voltage/ampere: 120 kV/35 mA, applied radiation dose: 55–60 mGy, time interval: 1 Sn, slice thickness: 0.6 mm. Evaluation windows are width (W): 80, length (L): 40 for brain, W: 2800, L: 600 for temporal bones, W: 350–400, L: 20–60 for soft tissues.

Double-blind evaluation method was used in the study. Cranial CTs were evaluated separately by 2 radiologists. If a discrepancy was found in the evaluation’s result, the cases were re-evaluated by both observers and a common consensus was achieved. The calcifications of fourth ventricle (CFV) were evaluated and classified according to anterior, posterior and lateral localisation. Both Boc FBCs were classified as unilateral and bilateral and the measurements were divided into three groups according to size of the calcifications: < 10 mm, between 5 mm and 10 mm, < 5 mm. If there was more than a 10% of difference between the sizes of the calcification, it was considered asymmetric, otherwise it was considered symmetrical. The morphological forms of the calcifications were also taken into account. They were classified into three different groups: linear, oval/nodular and conic. Besides, the presence of four common intracranial calcifications (calcifications of basal ganglion, habenular/pineal gland, choroid plexus, and vascular structures) was assessed. They were cross-matched with Boc FBC and associations were evaluated. The assessed calcifications are shown in Figure 1.

Figure 1. Box pilot figure shows age distribution of studied calcifications and study population; CFV — calcification of fourth ventricle; Boc FBC — calcification of foramen of Luschka/Bochdalek’s flower basket calcification.

Statistical analysis

The data were stored on a Microsoft Office Excel file (Excel 2010, Microsoft). Statistical software (SPSS, version 22.0, IBM) was used for analysis. Student’s t-test was used for the means of normally distributed data, and Mann-Whitney U test was used for parametric data that did not show normal distribution. Pearson c2 analysis was performed to evaluate the relationship between the categorical variables. P ≤ 0.05 was considered significant.

RESULTS

In 3.78% (10/264) of the patients wall CFV was found. Five of the them were located on the posterior wall, 3 on the anterior wall and 2 on the lateral wall. Five of these 10 patients had concomitant Boc FBC, and all of them were bilateral. Out of 10 patients with CFV, 9 had also choroid plexus calcifications, 9 had pineal and/or habenular gland calcifications, 3 had basal ganglia calcifications and 2 of them had vertebral artery calcifications. The mean age of the patients with CFV was 61.6 ± 19.05 years old and age range was 36–89 years old. Eight of the patients with CFV were males and 2 were females. There was statistically significant male predominance (p = 0.042).

Boc FBC was detected in 22.35% of our sample (59/264) (72.6 ± 12.9; 8–92 years old [age ± standard deviation; age range]). Out of 59 patients with Boc FBC, 5 (8.47%) had concomitant CFV. There was no statistically significant gender difference (p = 0.76). 69.5% of the Boc FBCs were bilateral. 53.7% of bilateral Boc FBCs were symmetrical while 46.3% of them were asymmetric. 52.6% of unilateral Boc FBCs was located at right while 47.4% were at left. 57.7% of the calcifications were < 5 mm, 25.4% of the calcifications were between 5 mm and 10 mm, 16.9% of the calcifications were > 10 mm.

Shapes of Boc FBC were evaluated. 37.3% of the patients had conic shaped Boc FBCs. Regarding the conical-shaped calcifications, the percentage of calcifications whose size was > 10 mm, 5 mm to 10 mm and < 5 mm was 45.5%, 31.8%, and 22.7%, respectively.

For the Boc FB calcifications whose size was < 5 mm, 41.2% were linear, 44.1% were oval or nodular and 14.7% were conic. For the Boc FB calcifications whose size was > 5 mm, the rates of linear and conic forms were respectively at 32% and 68%. Oval/nodular calcifications were not present in this group. Boc FBCs were accompanied by calcifications of basal ganglia, pineal/habenular, choroid plexus and vascular structures. The rates of these calcifications were respectively 20.3%, 94.9%, 93.2% and 39%. When only the patients with Boc FBCs were taken into account (n = 59), there were highly statistically significant correlations between Boc FBC and choroid plexus calcifications as well as pineal/habenular calcifications (p < 0.01) but this relationship was not mutual. Out of all patients (n = 264), basal ganglia, pineal/habenular, choroid plexus and vascular calcifications were seen respectively at the rate of 8.7% (23/264), 81.1% (214/264), 78.8% (208/264), 14.8% (39/264).

The rates of Boc FB in patients with basal ganglia calcifications and vascular structures calcifications were respectively 52.2% (12/23) and 59% (23/39). In the comparison to other intracranial calcifications, the correlations between Boc FB and calcifications of the basal ganglia/vascular structures were statistically significant (p < 0.05).

The rates of Boc FB in patients with pineal/habenular calcifications and choroid plexus calcifications were respectively 26.2% (56/214) and 26.4% (55/208). However, according to both Pearson c2 test and Whitney-Mann U tests, there was no statistically significant correlation for the latter (p > 0.05)

Demographic, morphometric findings and relation with other intracranial calcifications are shown in Table 1.

As for CFV, Boc FBC and total population, age was taken into account. The distribution of age groups from largest to smallest was respectively CFV > Boc FB > study population. The distribution is shown with a box plot graphic in Figure 1.

DISCUSSION

Boc FB is the overextension of the choroid plexus of the fourth ventricle towards the cerebellopontine angle. Bulbous terminal parts, also known as cornucopiae, are peripheral linear parts of Luschka where the choroid plexus is located and the farthest pieces that include choroid plexus tissue. Body and cornucopiae create an appearance similar to flower basket which gives the name of the anatomical structure [6]. Choroid plexus of the fourth ventricle originates from mesenchymal epithelium [19]. It is constituted by a central portion and lateral parts. The central portion is located on the posterior side of the fourth ventricle while the other parts cover the lateral faces [1, 13].

Anatomical definition is essential because calcifications occur in the same location as the choroid plexus. Foramen of Luschka is therefore a border between the lateral parts and Boc FB, if there is any [14, 24]. Boc FB was considered to be a blind-ending outward extension of the fourth ventricle choroid plexus when this structure was first described by Bochdalek. Later, it was understood that it includes linear structures [11, 19, 24].

In our study, we evaluated Boc FBC besides CFV. There was a significant difference between the frequency of Boc FBCs and CFV. While Boc FBCs were detected in 59 patients, only 10 patients had CFV. Boc FBC accompanied CFV in 50% of patients. But this relationship was not reciprocal. Out of all patients with Boc FBC, only 8.5% of patients had CFV. The samples are demonstrated in Figure 2.

Figure 2. A. Point calcification (arrowhead) on the posterior wall of the fourth ventricle in 56-year-old female patient; B. Bilateral linear calcification of foramen of Luschka/Bochdalek’s flower basket calcification (Boc FBC) in a 77-year-old female patient (cut arrowhead); C. A 84-year-old male patient with obvious circular left vertebral artery calcification (small arrowhead). Conical Luschka calcification on the left in a 65-year-old female patient (arrowhead).

Sharifi et al. [23] divided the Boc FBC into two parts which is similar to the definition of CFV. According to this study, the average choroid plexus extension after the foramen of Luschka was about 5–6 mm. However, according to our study, especially in elderly patients, Boc FBCs extend to 2 cm far from the centre. This different result shows that tortious basilar and vertebral artery calcifications can overlap with Boc FBCs in the cerebellopontine angle [23]. Bradac et al. [4] found symmetry between two sides of the choroid plexuses of the fourth ventricle in 96.5% of 57 brain dissections. Even though the choroid plexuses are symmetric, their calcification may not be symmetrical. In our study, CFVs were located at different points and asymmetric. Out of all the patients with Boc FBC, 30.5% had unilateral calcifications and only 53.7% of the patients that had bilateral calcifications presented symmetry.

Aneurysms, haemorrhages, cerebellopontine angle masses and tumours take part in the differential diagnosis of Boc FBCs on CT and MRI [11]. In our study, Boc FBCs were conical shaped with a rate of 37.29%. This shape is not an appearance seen in the pathologies cited above for the differential diagnosis. In the case of the conical-shaped calcifications being over 5 mm, the ratio significantly increased (17/25; 68%). Conical shaped calcifications were never detected among the vertebral artery calcifications seen in the same region. According to our study, conical form is not seen in every patient but it is evidence of Boc FBC if any. As far as we know, it is a new sign and there is no information about this sign in the literature.

It is well known that MRI is better in the demonstration of the choroid plexus. CT cannot show clearly Boc FB. However, CT is superior to MRI in the detection of calcifications. For this reason, we preferred non-contrast CT instead of MRI [11, 24].

Among the patients with Boc FBCs, 94.91% were over 60 years of age. No Boc FBC was found in the patients under 50; therefore, other diagnoses should be considered in this age group. In elder patients, vascular calcifications included in the differential diagnosis of Boc FBC are vertebral, basilar, anterior inferior cerebellar artery and posterior inferior cerebellar artery calcifications. Venous sinus calcifications may present similar appearances in the initial period. In younger patients, haemorrhages and calcified masses should be primarily considered in the differential diagnosis [5, 8–10, 21].

Intracranial calcifications are caused by calcium and iron deposition with ageing in especially highly vascularised localisations. They are almost always observed during CT examinations. In some cases, these can be linked to pathologies. However, they are often considered physiological when no concomitant disease can be identified [5, 7]. Since intracranial calcifications increase with age [2], they seem associated with the aging process [26].

Modic et al. [17] found that the incidence of lateral ventricular choroid plexus calcifications was 0.5% in the first decade and 86% in the eighth decade. In our study, Boc FBCs were compared with other intracranial calcifications. There is a high rate of association with choroid plexus calcifications and habenular/pineal calcifications. The association rate of Boc FB with choroid plexus calcifications, habenular/pineal calcifications, vertebral calcifications and basal ganglia calcifications was respectively 94.9%, 93.2%, 39.0%, and 20.3%.

Let’s point that heterotopic ossification is a different entity that must be differentiated from calcifications. It refers to a large amount of bone and is seen mainly in the extremities. However, heterotopic ossifications may occur because of thermal traumas and surgical procedures of the intracranial region in the head or in soft tissue [20].

The study has some limitations. First, the study was retrospective and a limited number of patients had both MRI and CT; therefore, Boc FBCs were only assessed from CT and the volume of Boc FB omitted. Secondly, since the article length is limited, only the most common four intracranial calcifications were chosen and compared with Boc FBC.

CONCLUSIONS

There are very limited studies about Boc FB and its calcifications. In other words, Boc FBCs are an underreported finding in the literature. This entity is important because it can be confused with very important pathologies like haemorrhage or calcified masses. Although, it is reported that Boc FBs are symmetrical, according to our results their calcifications are rarely symmetrical. This condition has increased the margin of error. According to our study’s results, Boc FBCs are seen in the advanced age group and re not encountered under the age of 50. The conical form is seen in one-third of the cases but it is a very beneficial finding for distinguishing Boc FBC from other calcifications, if any. The advanced age group calcifications especially choroid plexus calcifications and pineal/habenular calcifications are highly associated with Boc FBC. In the case of the presence of CFV, Boc FBCs accompany at a high rate.

Conflict of interest: None declared