Neuroradiology

, Volume 59, Issue 3, pp 213–219 | Cite as

Analysis of the venous channel within the clivus using multidetector computed tomography digital subtraction venography

  • Katsuhiro Mizutani
  • Masahiro Toda
  • Jun Kurasawa
  • Takenori Akiyama
  • Hirokazu Fujiwara
  • Masahiro Jinzaki
  • Kazunari Yoshida
Diagnostic Neuroradiology

Abstract

Purpose

Although neuroradiologists and skull base neurosurgeons are aware of the existence of veins within the clivus, such vessels have seldom been described in the literature. The aim of the present study is to elucidate the detailed venous structure of the clivus.

Methods

Computed tomography digital subtraction venography (CT-DSV) images of 50 unruptured aneurysm cases were examined retrospectively.

Results

Eighteen emissary veins were identified in 14 (28.0%) cases. A half of the emissary veins connected the inferior petrosal sinus with the inferior petro-occipital vein (IPOV) in the middle clivus. The clival diploic vein (CDV) was identified in 14.0% of cases, 42.9% of which had the clivus of the presellar type. The CDV was connected to the posterior intercavernous sinus or the rostral end of the basilar plexus superiorly, and was connected to the IPOV, anterior condylar vein, marginal sinus, or the anterior condylar confluence.

Conclusion

The CDV provides collateral channels between the cavernous sinus and the internal jugular vein and the inferior petrosal sinus and the IPOV. Understanding of the emissary veins in the clivus and the CDV is valuable for skull base surgery, especially for endonasal endoscopic skull base procedures.

Keywords

Clival diploic vein Clivus Endonasal endoscopic skull base surgery Emissary vein 

Introduction

The recent development of endonasal endoscopic skull base surgery has enabled access to clivus lesions [1, 2, 3, 4, 5]. Drilling of the clivus during extended trans-sphenoidal surgery for parasellar lesions is often accompanied by bleeding. Although neuroradiologists and neurosurgeons are aware of the existence of diploic or emissary veins within the clivus [6], the detailed venous structure remains unknown. Therefore, the aims of the present study are to elucidate the venous structure within the clivus using computed tomography digital subtraction venography (CT-DSV) and to present its anatomical features. Information on veins within the clivus, which is the focus of this article, can be useful for neuroradiologists and neurosurgeons, and especially for skull base neurosurgeons.

Methods

Patients

Fifty patients (15 men and 35 women; age 37–82 years, average age 62.4 years) with intracerebral aneurysm but otherwise normal anatomy were included in the present study. All patients underwent CT-DSV evaluation before clipping surgery or coil embolization. One case of skull base meningioma was also included in order to present an illustrative example of a clival diploic vein.

Computed tomography digital subtraction venography technique

CT-DSV was performed with a CT scanner (Aquilion ONE; Toshiba Medical Systems Corporation, Otawara, Tochigi Prefecture, Japan) equipped with 320 detector rows. Initially, a test bolus scan was performed at the level of the carotid bulb in order to determine the optimal timing of dynamic scans using an intravenous injection of 10 mL of nonionic contrast medium (Iopamiron®, 370 mg/ml) at a rate of 5 mL/s, followed by 20 mL of saline. Subsequently, CT digital subtraction angiography (DSA) scans were obtained after a bolus injection of 50 mL of contrast medium at a rate of 5 mL/s, followed by 20 mL of saline. The CT-DSA scans consisted of a volume scan before the arrival of contrast medium to obtain an unenhanced mask volume data set for subsequent bone subtraction, three arterial phase volume scans over 5 s (rotation time 1 s), and one venous phase scan (10.5 s after the initial arterial phase). Other scan parameters were as follows: field of view, 25 cm; slice thickness, 0.5 mm; tube voltage, 120 kV; and current-time product, 200 mAs (mask phases) and 100 mAs (other phases). CT-DSV images were obtained from the mask and the venous phase images. Volume-rendering images of the arterial and venous phases were superimposed on bone images of the skull base to improve the recognition of the skull base vascular anatomy. This CT-DSV technique was similar to those used in previous reports from our facilities [7, 8].

Image analysis

The sphenoid sinus types in the clivus was classified into three groups (conchal, presellar, and sellar) based on the extension of pneumatization around the sella turcica [9]. The sinus pneumatization types were judged on the midsagittal images. In the conchal type, the sphenoid sinus is separated from the sella turcica. In the presellar type, the pneumatization of the sphenoid sinus does not pass across the line between the tuberculum sellae and the anterior wall of the sella turcica. In the sellar type, the sphenoid sinus reaches the line between the tuberculum sellae and the anterior wall of the sella turcica. The clivus was divided into upper, middle, and lower thirds by two endocranial landmarks: the dural pori of the abducens nerves and the dural meati of the glossopharyngeal nerves [10]. The upper clivus and the middle clivus were separated by the axial plane of Dorello’s canal. The middle clivus and the lower clivus were separated by the axial plain of the glossopharyngeal meatus. The upper and middle regions of the clivus mostly face the pons, while the lower part mostly faces the medulla. In cases with unruptured aneurysm, the existence and route of the veins within the clivus were evaluated on axial CT-DSV images by a neurosurgeon and a neuroradiologist. An emissary vein was defined as a venous channel penetrating the clivus and connecting an intracranial channel with an extracranial venous channel. A longitudinal vein within the clivus was considered as a clival diploic vein (CDV). We also evaluated these veins in one case of skull base meningioma.

Statistical analysis

Correlations of discrete and categorical variables were analyzed using Fisher’s exact test. The Student t test was used for continuous variables. P values of <0.05 were considered to indicate statistically significant differences.

Results

The conchal, presellar, and sellar types of clivus were observed in one (2.0%), four (8.0%), and 45 (90.0%) cases, respectively.

In 14 cases (28.0%), we detected 18 emissary veins. Two emissary veins were detected in four cases. Sphenoid sinus types did not influence the existence of emissary veins. The emissary vein was located in the lower clivus in five cases, and in the upper clivus in three cases. Ten emissary veins were found in the middle clivus in nine cases.

The emissary veins ran horizontally and connected the intracranial inferior petrosal sinus, marginal sinus, or basilar plexus with the extracranial IPOV or veins located in the pharynx. In one case, the emissary vein in the upper clivus connected the cavernous sinus with the IPOV. Nine emissary veins in the middle clivus connected the inferior petrosal sinus (IPS) with IOPV. Bilateral IPSs were demonstrated in all patients except one case with the emissary vein. Bilateral IPOVs were observed in 11 out of the 14 cases with emissary veins (78.6%) and 19 of 36 cases without emissary veins (47.252.8%, p =0.12). A summary of the cases with the emissary veins is shown in Table 1. In one case, we detected the vein penetrating the upper clivus horizontally, similar to emissary vein. However, the vein connected the intracranial basilar plexus with the intracranial posterior intercavernous sinus and did not match the definition of the emissary vein in the present study.
Table 1

Summary of the cases with emissary veins

Case No.

Age

Sex

Sellae type

IPSa

IPOV

Emissary Veins

L

R

L

R

Upper

Middle

Lower

Connection (side)

L

M/P

R

L

M/P

R

L

M/P

R

 

4

61

F

S

+b

+

+

+

    

+

    

BP(M/P)-Pha (M/P)

5

63

F

S

+

+

+

+

        

+

MS(R)-IPOV(R)

8

55

F

P

+

+

+

+

+

        

CS(L)-IPOV(L)

     

+

   

IPS(R)-IPOV(R)

12

67

M

S

+

+

+

+

     

+

   

IPS(R)-IPOV(R)

14

73

M

P

+

+

+

+

+

        

BP(L)-Pha(L)

25

69

F

S

+

+

+

+

   

+

     

IPS(L)-IPOV(L)

        

+

MS(R)-IPOV(R)

27

55

F

S

+

+

+

+

     

+

   

IPS(R)-IPOV(R)

30

63

M

S

+

+

+

+

   

+

     

IPS(L)-IPOV(L)

     

+

   

IPS(R)-IPOV(R)

37

65

M

S

 

+

 

+

     

+

   

IPS(R)-IPOV(R)

38

77

F

S

+

+

+

+

      

+

  

BP(L)-Pha(L)

40

70

F

S

+

+

+

+

     

+

   

IPS(R)-IPOV(R)

      

+

  

MS(L)-IPOV(L)

41

58

M

S

+

+

 

+

        

+

IPS(R)-IPOV(R)

46

62

F

S

+

+

 

+

  

+

      

IPS(R)-IPOV(R)

48

63

F

S

+

+

+

+

   

+

     

IPS(L)-IPOV(L)

 

Total (14 cases)

      

2

0

1

3

1

6

2

0

3

 

a F female, M male, S sellar type, P presellar type, L left, M/P median/paramedian, R, right, BP basilar plexus, IPS inferior petrosal sinus, Pha pharyngeal vein, MS marginal sinus, IPOV inferior petro-occipital vein, CS cavernous sinus

b“+” indicates that the corresponding vein was present. For example, in the case 4, there were bilateral IPS and IPOV as well as an emissary vein in the median/paramedian clivus, which connected the intracranial basilar plexus with the pharyngeal vein

In seven cases (14.0%), we detected a longitudinal vein within the clivus and named it the clival diploic vein (CDV). Its rostral end was connected to the posterior intercavernous sinus in two cases and the most superior portion of the basilar plexus in five cases. The CDV ran inferiorly near the midline and typically diverged into two veins in the middle clivus and then ran inferolaterally within the lower clivus. In four cases, the vein did not diverge and was present on one side only. Therefore, in the present case series, there were 10 distal ends of the CDV, which were connected to the anterior condylar confluence (ACC, n = 1; 10.0%), anterior condylar vein (n = 1; 10.0%), IPOV (n = 7; 70.0%), and the marginal sinus (n = 1; 10.0%). Six ends of the CDV exited the clivus at the level of the foramen lacerum in the middle clivus and were connected to the IPOV via the internal carotid artery venous plexus of Rektorzik. The remaining four ends of the CDV ran relatively long within the clivus and were connected to the ACC, anterior condylar vein, IPOV, or marginal sinus. The CDV was present in 3 (75.0%) out of the 4 cases of the presellar type and in 4 (8.7%) out of the 46 cases of the sellar type (p = 0.007). The luminal diameter of the detected CDV ranged from 1.2 to 4.5 mm (mean: 2.24 mm) on CT-DSV. The case with the most prominent CDV is shown in Fig. 1, where the CDV is easily detectable by non-subtraction enhanced CT and flow void in the MR scan. In most cases, the channels were less developed than in the prominent case illustrated in Fig. 1 and were only detectable by CT-DSV. All the cases with a CDV had bilateral IPSs and bilateral IPOVs. In two cases (case 8 and 14 in tables), the emissary veins were connected to the CDV in the middle (case 8) or upper clivus (case 14). A bony structure surrounding the CDV was identified in only one case on non-enhanced CT (Fig. 1H). A summary of the cases with a CDV is shown in Table 2.
Fig. 1

Radiological images of the clival diploic vein. ag The clival diploic vein (CDV) is shown in 3-dimensional volume-rendering images of computed tomography (CT) angiography. (H): non-enhanced CT image; (I): T2 weighted image. All images are from one patient. In this case, a well-developed CDV arises from the superior side of the basilar plexus (a, b). It runs within the clivus and diverges into two veins at the level of the pons (d, e). Each vein runs inferolaterally and is eventually connected with the anterior condylar confluence on the right side and with the anterior condylar vein on the left side. The inferior petro-occipital veins are also observed (f, red arrow). A bony canal is observed on non-enhanced CT, in which the CDV runs (H, yellow arrow). If the CDV develops well, it can be seen as a flow void in magnetic resonance (MR; I, white arrow)

Table 2

Summary of the cases with a clival diploic vein (CDV)

Case no.

Age

Sex

Sellae type

IPSa

IPOV

Clival diploic vein

L

R

L

R

Rostral connection

Caudal connection

Bone canal

Connection with emissary vein

L

R

  

2

61

F

P

+

+

+

+

BP

IPOV

IPOV

  

8

55

F

P

+

+

+

+

BP

ACV

ACC

+

+

14

73

M

P

+

+

+

+

PICS

IPOV

IPOV

 

+

15

72

M

S

+

+

+

+

BP

 

IPOV

  

24

74

M

S

+

+

+

+

PICS

 

IPOV

  

39

68

F

S

+

+

+

+

BP

MS

   

47

67

F

S

+

+

+

+

BP

IPOV

   

a F female, M male, P presellar, S sellar, L left, R right, BP basilar plexus, PICS posterior intercavernous sinus, ACV anterior condylar vein, ACC anterior condylar confluence, IPS inferior petrosal sinus, MS marginal sinus, IPOV inferior petro-occipital vein

All the cases had bilateral IPSs and bilateral IPOVs. The bony structure surrounding the CDV was identified in only one case

Patient demographics, such as age or sex, did not influence the rate of detection of emissary veins or CDVs (data not shown). A typical connection of a CDV with surrounding venous structures is shown in Fig. 2.
Fig. 2

Schematic illustration of the clival diploic vein and surrounding venous structure (superoposterior view). This illustration demonstrates the connections of the clival diploic vein (CDV) (highlighted by yellow) with the surrounding venous structure, such as the posterior intercavernous sinus, basilar plexus, inferior petro-occipital vein, anterior condylar vein, marginal sinus, and anterior condylar confluence. AICS anterior intercavernous sinus, PICS posterior intercavernous sinus, CS cavernous sinus, BP basilar plexus, SPS superior petrosal sinus, Sigmoid sigmoid sinus, ICA internal carotid artery, VP of Rektorzik internal carotid artery venous plexus of Rektorzik, IPOV inferior petro-occipital vein, IPS inferior petrosal sinus, ACC anterior condylar confluence, CDV clival diploic vein, ACV anterior condylar vein, IJV internal jugular vein, JF jugular foramen, HGC hypoglossal canal, MS marginal sinus, F. Lacerum, foramen lacerum

Illustrative case of a clival diploic vein

A 74-year-old woman presented at a local hospital with depression and gait disturbance. MRI (Fig. 3a) revealed a massive petroclival cavernous tumor that compressed the temporal lobe, brain stem, and cerebellum. While her bilateral IPSs were not visualized by CT-DSV, CDVs were well developed and connected the distal portion of the basilar plexus to the bilateral ACC (Fig. 3c–h). The connection between the left cavernous sinus and the left pterygoid plexus was undeveloped. In this case, the CDVs functioned as a collateral channel between the left superficial middle cerebral vein and the internal jugular veins. Before carrying out CT-DSV, we considered performing tumor decompression via the trans-sphenoidal approach; however, because this presented a risk of injury to the CDV and impairment of cerebral drainage, we planned to perform the anterior transpetrosal approach but decided against it because of the patient’s condition and the wish of the patient’s family.
Fig. 3

Clival diploic vein in a case of petroclival meningioma. a Enhanced T1 weighted image. b Non-enhanced computed tomography axial image, the same level as e. ch Computed tomography digital subtraction venography (CT-DSV) image. In this case, the bilateral inferior petrosal sinuses (IPSs) are not visualized because of the invasion of the petroclival cavernous meningioma (T) (a). A well-developed clival diploic vein (CDV, white arrow) is observed by CT-DSV (ch). In the non-enhanced CT image (b) at the same level as (e), the CDV runs through the clivus. In this case, the distal part of the CDV is connected to the laterocavernous sinus via the basilar plexus (c), and its proximal part runs inferiorly to the petro-occipital fissure and is connected to the anterior condylar confluence

Discussion

Emissary veins

The emissary veins in the clivus have been described in a single report as transclival emissary veins connecting the basilar venous plexus to veins on the inferior surface of the vlivus adjacent to the pharynx [6]. In the present study, emissary veins were identified in 28.0% of cases. The emissary veins connected the basilar plexus or the inferior petrosal sinus to the venous channels located on the inferior surface of the clivus. A bilateral IPOV tended to be present more often in cases with emissary veins than in cases without emissary veins. In many cases, the emissary veins located in the middle clivus (10/18, 55.6%), and 15 emissary veins (15/18, 83.3%) were connected to the IPOV (Table 1).

Clival diploic vein

In the present study, the CDV ran within the clivus and connected the veins on the dorsal sellae, such as the posterior intercavernous sinus or basilar plexus, with the IPOV, ACC, marginal sinus, or anterior condylar vein. While the IPOV is generally superiorly connected to the internal carotid artery venous plexus of Rektorzik [11, 15] and is linked to relatively lateral aspects of the cavernous sinus, the CDV is rather continuous to medial aspects of the cavernous sinus via the basilar plexus or the posterior intercavernous sinus. Three quarters of the cases with the clivus of the presellar type had CDVs with similar courses within the clivus. Therefore, the CDV seems to have a relatively stable anatomical structure in the presellar-type clivus.

Few studies have documented clival diploic veins [11, 12, 13], and their longitudinal courses have not been reported. Schntizlein et al. described the sinus of the dorsum sellae [13]. Its location was correlated with that of a part of the CDV. It was continuous anteriorly and laterally with the cavernous sinuses, posteriorly and laterally with the superior and inferior petrosal sinus, and inferiorly with the basilar plexus. Its posterior wall was a thin cortical bone and/or dura, but anteriorly it was within the clivus [13]. According to the authors, the sinus of the dorsum sellae was comparable to the basivertebral vein within the bodies of the vertebrae. From this description, its location appears to be limited to the most superior portion of the clivus, and neither it nor the basivertebral veins run along the longitudinal axis. We suggest that the sinus of the dorsum sellae may be an enlarged emissary vein or a part of the CDV or basilar plexus.

Embryologically, the CDV appears to be formed before the ossification of the clivus because it is penetrated by the CDV. The clivus is formed inferiorly of the pars basilaris of the occipital bone and superiorly of the basisphenoid of the sphenoid bone [16]. At around 40 days of fetal life, the loose mesenchyme surrounds the primitive brain [17]. This mesenchyme layer is referred to as the primary meninx, which in later stages differentiates into the pia mater, dura mater, and skeletogenous layers. From this outermost skeletogenous layer, the cartilaginous craniums, including the clivus, are formed [16, 18]. Ossification of the pars basilaris of the occipital bone occurs between the eleventh and twelfth weeks of fetal life [16], whereas ossification of the basisphenoid of the sphenoid bone takes place between the thirteenth and sixteenth weeks [16]. The formation of the clivus is completed after the closure of the spheno-occipital synchondrosis at an age of 13–18 years [16, 18].

The IPS and basilar plexus are close in venous structure to the CDV and run longitudinally along the dorsal surface of the clivus. Padget et al. described these venous structures as being formed from the venous plexiform within the future dural layer at no later than 10 weeks of fetal life [19, 20]. Although Padget et al. did not mention the CDV in their report, we hypothesize that it is also formed from the plexiform venous network within the primitive skeletogenous layer before the tenth week of fetal life and later remains within these ossified bones. Various connections between surrounding venous channels, such as the basilar plexus, posterior intercavernous sinus, and ACC, may reflect the embryological plexiform network within the primitive dural layer. Interestingly, we detected a CDV significantly less often in the cases with the clivus of the sellar type, and the past reports have not identified the sinus of the dorsum sellae in cases with pneumatization of the dorsum sellae [13]. We hypothesize that, in some patients with the clivus of the sellar type, CDVs may originally be present but are lost after birth because of pneumatization and thinning of the clivus, which eliminates a site for venous structures, including the CDV.

The main reason why the CDV has not been recognized so far is the difficulty in its detection in cadaver and conventional digital subtraction (DSA) studies. In cadavers, the small channel within the bone does not allow for easy detection of vessels other than the superficial cortical or dural veins [14]. In DSA, larger vascular structures adjacent to the CDV, such as the inferior petrosal sinus or the basilar plexus, interrupt its visibility in the anteroposterior and lateral views. At present, CT-DSV is the best method for detecting small vasculature within the clivus.

Clinical applications

The emissary veins and CDVs are located in the clivus and can cause hemorrhage, air embolism, and postoperative epidural hematoma if the endonasal transclival approach is used. In cases with well-developed emissary veins and CDV, extra caution is necessary during drilling of the clivus. Since several routes connect the cavernous sinus and the internal jugular vein, its transection during the operation does not seem to cause venous congestion, except in cases of deficit of the IPS and/or IPOV. However, when the CDV is mainly responsible for intracerebral drainage (as seen in Fig. 3), its loss may cause severe venous congestion. Therefore, existence of a CDV sustaining cerebral drainage can be a contraindication for the endonasal transclival approach.

Similar to the IPOV [21], a well-developed CDV can be used as an alternative venous route to the cavernous sinus.

Conclusions

In the present study, we analyzed the clival emissary and clival diploic veins by CT-DSV. Detailed knowledge of these vessels can be useful when performing cranial base surgery, especially endonasal endoscopic skull base surgery.

Notes

Acknowledgments

The authors thank Dr. Masaki Komiyama and Dr. Hiro Kiyosue for their advice on neurovascular anatomy and embryology.

Compliance with ethical standards

We declare that all human and animal studies have been approved by the ethics committee of Keio University School of Medicine and have therefore been performed in accordance with the ethical standards laid down in the 1964 Declaration of Helsinki and its later amendments. We declare that all patients gave informed consent prior to inclusion in this study.

Conflict of interest

We declare that we have no conflict of interest.

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Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Department of NeurosurgeryKeio University School of MedicineTokyoJapan
  2. 2.Department of RadiologyKeio University School of MedicineTokyoJapan

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