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ORIGINAL ARTICLE
Year : 2022  |  Volume : 70  |  Issue : 4  |  Page : 1506-1511

A Transvenous Endovascular Approach in Straight Sinus has Minor Impacts on Chordae Willisii


1 Department of Neurosurgery, Liuzhou People's Hospital, Liuzhou, Guangxi Autonomous Region; Department of Neurosurgery, Zhujiang Hospital, Southern Medical University, Guangzhou, China
2 Department of Forensic Medicine, Guizhou Medical University, Guiyang, Guizhou, China
3 Department of Neurosurgery, Liuzhou People's Hospital, Liuzhou, Guangxi Autonomous Region, China
4 Department of Research, The Bioillus Institute of Technology, Guangzhou, Guangdong Province, China
5 Department of Anatomy, Guangxi Medical University, Nanning, Guangxi Autonomous Region, China
6 Department of Cerebrovascular Surgery, The Third Affiliated Hospital, Sun Yat-Sen University, Guangzhou, Guangdong Province, China

Date of Submission10-Jun-2020
Date of Decision14-Jul-2021
Date of Acceptance14-Jul-2021
Date of Web Publication30-Aug-2022

Correspondence Address:
Qiujing Wang
Department of Cerebrovascular Surgery, The Third Affiliated Hospital, Sun Yat-Sen University, Guangzhou - 510630, Guangdong Province
China
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/0028-3886.355179

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 » Abstract 


Background: The transvenous endovascular approach has become an optimal method for the treatment of cerebrovascular diseases. This procedure might cause iatrogenic damage to the chordae willisii (CW) in the straight sinus. However, little literature has been found to support this hypothesis.
Objective: To investigate the possible damage of CW in the straight sinus during a transvenous endovascular procedure.
Materials and Methods: The features of the CW from 38 cadaveric heads were observed via an endoscope mimicking a mechanical thrombectomy procedure in the straight sinus. Endoscopic observation and light microscopy examination were used to assess the damage of the CW throughout the procedure.
Results: Valve-like lamellae and longitudinal lamellae were found predominantly in the posterior portion of the straight sinus. Trabeculae were present in both the anterior and posterior portions of the straight sinus. Samples treated with a stent had a significantly higher rate of Grade 1 damage during the eight procedures compared with samples treated with a balloon (P = 0.02). The incidence of damage to the CW surface was higher in the stent group than in the balloon group (P = 0.00). The use of stent or balloon did not increase the rate of CW damage during repeated experiments.
Conclusions: The stent or balloon navigation through the straight sinus can cause minor damage to the CW. Frequent uses of retrograde navigation through the straight sinus do not seem to increase the possibility of damage to CW.


Keywords: Chordae willisii, endoscopy, intervention, straight sinus, venous sinus thrombosis
Key Message: Minor damages to the Chordae willisii occur while stent or a balloon are navigated through the straight sinus.


How to cite this article:
Ye Y, Ding J, Liu S, Wen G, Huang S, Wang Q. A Transvenous Endovascular Approach in Straight Sinus has Minor Impacts on Chordae Willisii. Neurol India 2022;70:1506-11

How to cite this URL:
Ye Y, Ding J, Liu S, Wen G, Huang S, Wang Q. A Transvenous Endovascular Approach in Straight Sinus has Minor Impacts on Chordae Willisii. Neurol India [serial online] 2022 [cited 2022 Oct 7];70:1506-11. Available from: https://www.neurologyindia.com/text.asp?2022/70/4/1506/355179

Yuanliang Ye and Jiuyang Ding contributed equally to this work.




Cerebral vascular diseases, such as vascular malformation[1],[2] and thrombosis,[3],[4] involve the straight sinus (SS). Patients with straight sinus thrombosis experienced poor outcomes for bilateral thalamic hemorrhagic infarction.[5],[6] The transvenous endovascular approach is considered a first-line treatment for these diseases.[3],[7] This intravascular intervention might cause iatrogenic damage to the chordae willisii (CW), which exists in the SS and upon damage, would expose its collagen fibers and cause thrombosis. However, little literature has been found to support this hypothesis. During a transvenous endovascular thrombectomy procedure conducted at the Zhujiang Hospital of Southern Medical University, we encountered various amount of resistance in the SS [Video 1]. Although administered with standardized anticoagulant therapy, the patient still experienced recurrence of thrombosis two weeks after surgery [Figure 1]. Confirmed that there was no venous stenosis in the SS, we suspected that the resistance we encountered could be caused by anatomical structures within the sinus. We speculated that the damage to internal structures in the SS might result in the exposure of collagen fibers, which activated a coagulation mechanism and contributed to thrombosis recurrence.
Figure 1: The device was seemingly resisted by some anatomical structure within the sinus (b). No resistance was experienced when the stent moved through both AnSS and TS (a and c). Although low-molecular-weight heparin and warfarin were used after surgery, the patient's consciousness returned to lethargy with recurrence of SS thrombosis (white circle) in 2 weeks after surgery (e). The illustration of suspected causes of resistance in the SS (d)

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Imaging and standard anatomical methods have already been used to study the anatomical structure of the SS.[8],[9],[10] For instance, using ultrastructural analysis, the SS composition and the possibility of SS constituent layer dissection has been extensively described.[11],[12],[13],[14] Endoscopic methods are well-established and routinely utilized to examine the internal structures of the superior sagittal sinus (SSS).[15],[16] In the present study, we performed a high-definition rigid endoscopic procedure in the SS of cadavers by mimicking a mechanical thrombectomy (MMT) process. We observed CW in the SS and its morphological feature. The damage to CW via the endoscopic procedure was assessed through observations during the procedure and later by light microscopy.


 » Materials and Methods Top


A total of thirty-eight cadaveric heads were obtained from autopsies performed at the Department of Anatomy, Guangxi Medical University. The consent of usage form was signed by the donor or the relatives of the donors who were all above age 18. This study was approved by the ethics committee of Southern Medical University Zhujiang Hospital and Guangxi Medical University. All cadaveric heads were fixed in 10% formalin solution for 4–8 weeks. The exclusion criteria were as follows: 1) craniocerebral trauma, 2) neurological disease, and 3) disease affecting the dural sinuses.

Assessment of morphological characteristics of the chordae willisii by endoscopy

Twenty-two cadavers were used in the endoscopic assessment of the CW in SS for the observational and descriptive study. The relevant clinical data included gender, age, height, weight, comorbidities, and cause of death. The mean age of these specimens was 65 ± 13.19 years old (range: 43–83 years), and they included 14 male and 8 female. Latex was not injected into veins or dural sinus. The scalp was removed with particular attention to exposing the inion. The occipital bone around the inion was removed using a Rongeur until the confluence of sinuses and the bilateral transverse sinuses were completely exposed. Then, the brain tissue around the SS was resected en-bloc, whereas brain tissue around the junction between the great cerebral vein and SS was subpially removed in a piecemeal fashion. A 4.5-gauge needle pointed to the confluence of sinuses was inserted into the inferior sagittal sinus. The SS and SSS was flushed with tap water to remove blood clots. A high-definition rigid endoscope (Karl Storz, German) measuring 2.7 mm in diameter and optics (0° and 30°) was inserted into the lumen of the SS and SSS from the confluence of sinuses.

Mimicking mechanical thrombectomy in the SS

Sixteen cadaveric heads were used to evaluate the damage by MMT to CW in the SS. The mean age of these specimens was 61 ± 12.48 years old (range: 41–79 years), and they included 4 male and 12 female specimens. A 6-F Envoy guide catheter (Cordis, Inc., Miami, FL, USA) was placed at the transition from transverse to sigmoid sinuses via the left or right posterior mastoid bone window. In the balloon group, a micro guidewire and a microcatheter were advanced retrogradely into the junction between the great cerebral vein and the SS. After the position of the catheter was confirmed using poster-anterior and lateral projection DSA radiography, the tip of the micro guidewire was kept in the anterior third of the SS. The micro catheter was pulled out and replaced by a 5-mm rapid exchange balloon reaching to the anterior third of the SS along the micro guidewire. In the stent group, a 4–20 mm Trevo Pro Vue stent retriever was delivered to the anterior third of the SS along the microcatheter. The dilated balloon or the stent was slowly pulled back to the sigmoid sinus. These processes were repeated three times.

Assessment of damage to the chordae willisii by endoscopy

Damage to the CW was evaluated using an endoscope, which was inserted into the lumen of the SS from the confluence of sinuses. Based on the degree of damage to the CW, the following classification system was used in this study: Grade 0: no damage; Grade 1: broken off at the surface of the CW; Grade 2: split away from the CW completely [Table 1].
Table 1: Simple damage classification system of CW during mimicking mechanical thrombectomy in the SS

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Assessment of damage to the chordae willisii by light microscopy

After tissue preparation, samples from the SS were subjected to microscopic examination. H and E and Masson's trichrome (for collagen fiber) staining methods were utilized. The sections were examined using a Zeiss Axioskop Plus microscope (Carl Zeiss Microscopy) at 50×, 100×, and 400× magnifications. Images were acquired and stored by Axio Vision software. The following classification system was used to record the microscopic damages: Grade 0: endothelial lining and collagen fibers remain intact; Grade 1: partial damage to endothelial cell or collagen fibers; Grade 2: both endothelial cell and collagen fibers were completely damaged [Table 1].

Statistics

All statistical analyses were performed using SPSS 22 for Windows (SPSS Inc., Chicago, Illinois). Categorical data, including the number of CW and the percentage of coverage, were summarized using descriptive statistics. The numerical data were summarized as means ± SDs. Independent-sample Student's t-test was used to compare the distribution of CW in different segments of the SS. The nonparametric independent sample test was used to compare the numbers of CW between SS and SSS. The nonparametric Chi-square was also used to compare the damage to the CW between the balloon group and the stent group. A P value of <0.05 was considered statistically significant.


 » Results Top


Types of chordae willisii in the SS

There were 213 CWs altogether in 22 examined SS; the highest number in one SS was 14, and the lowest 6. Details related to the number of CWs are shown in [Table 2]. The most common and numerous type of CW was the valve-like lamellae that made up 41.31% of all CWs in the examined straight sinuses. The openings of most valve-like lamellae were found mainly in the posterior portion of the SS and located at the junction between the lateral and inferior wall (IW) of the sinuses [Figure 2]a. The trabeculae, which made up 32.39% of all CWs in our study, were the second most common form of CW in the SS. The trabeculae could be seen either centrally or peripherally in the lumen appearing as either solitary or clustered structures [Figure 2]b. Laminar chordae, which divided the lumen of the straight sinus into different diameters, were the least common form of CWs. Laminar chordae were observed either in the orifice or in the middle of the straight sinus and ran in horizontal, perpendicular, or oblique directions [Figure 2]c. A nodule was found at the junction between the great cerebral vein and the SS [Figure 2]d. Valve-like lamellae and longitudinal lamellae were found predominantly in the posterior portion of the straight sinus (PoSS) [Figure 2]e and [Figure 2]f. However, trabeculae were present in both the anterior and posterior portions of the straight sinus as well [Figure 2]g.
Figure 2: Endoscopic view of the CW. A valve-like chorda willisii was located at the junction between the LW and IW (a). Two trabeculae in the lumen of the SS (b). A longitudinal chordae inside the sinus, which divided the lumen into two channels. A valve-like chorda is present in the channel (c). Nodule present at the junction between the great cerebral vein and the SS (d). Graphs showing comparisons of the number of valve-like lamellae (e), trabeculae (f), and longitudinal lamellae (g) in the AnSS and PoSS

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Table 2: Comparison of the number of chordae willisii between straight sinus and superior sagittal sinus

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Comparison of the number of chordae willisii to SSS

The number of CWs in each SS and SSS was 9.92 ± 1.85 and 16.90 ± 2.57, respectively. There was a significance difference in the number of CWs between SS and SSS (P = 0.00). There was no difference in the distribution of valve-like lamellae, trabeculae, and longitudinal lamellae between SS and SSS (P = 0.836).

Effect of stent/balloon damages to chordae willisii observed by endoscopy

The damage to CW by either the stent or the balloon was recorded with a system wherein Grade 0 indicated minimum damage and Grade 2 maximum. In the stent group, the number of cases with Grade 0, Grade 1, and Grade 2 was 26 (53.1%), 21 (42.9%), and 2 (4.10%), respectively. The use of stent resulted in no significant increase in damage to CW during the three replicated procedures (P = 0.511). In the balloon group, there were 34 (73.9%) cases showing Grade 0, 8 (17.4%) Grade 1, and 4 (8.7%) Grade 2. The use of a balloon also resulted in no significant increase in damage to CW during the three replicated procedures (P = 0.88) [Figure 3].
Figure 3: Effect of a stent/balloon on the CW in the SS. The stent was delivered to the anterior third of the SS along a microcatheter (a). Damage of Grade 1 (b) was observed by endoscopic view. Graphs showing comparisons of the damage to the CW among three replicates in the stent group (c). The balloon was delivered to the SS, dilated and drawn slowly back to the sigmoid sinus (d). Grade 2 damage was observed by endoscopy (e). Graphs showing comparisons of the damage to the CW among three replicates in the stent group (c) and the balloon group (f)

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There were no significant differences in the distribution of damage in both groups (P = 0.10). Based on our observation, damage to CW in the SS happened at two locations: the surface and junction (between IW and lateral wall). The incidence of damage to the surface of CW was higher in the stent group than in the balloon group (P = 0.00).

Effect of the stent/balloon damages to chordae willisii observed by microscopy

Histological staining of the Grade 0 cases revealed the presence of an endothelial lining with patent cell nuclei [Figure 4]a. Subendothelial connective tissue containing collagen fibers and vessels were also observed [Figure 4]b. No smooth muscle fibers were observed in the CW. Histological staining also revealed a fissure at the surface of the CW in every Grade 1 case [Figure 4]b and complete fragmentation of the CW in every Grade 2 case [Figure 4]c. The use of stent resulted in a significant increase in Grade 1 damage in the eight specimens than that observed in the balloon group (P = 0.02) [Figure 4]d.
Figure 4: The morphological characteristics of intraoperative damage to the CW observed by microscopy. At Grade 0, the CW predominantly consists of collagen tissue and endothelial cells (HE, 100×) (a). In a Grade 1 case, histopathological coronal sections showed the damage of endothelial cells (black arrow) and small area collagen fiber exposure (b). In a Grade 2 case, a large area of collagen fiber (square) was exposed completely (HE, 100×) (c). Graphs showing comparisons of the damage to the CW between the stent group and the balloon group (d)

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 » Discussion Top


In this study, we observed the presence and morphological features of the CW in the SS and assessed the degree of damages to the CW by either stent or balloon via endoscopic observation and histological investigation. We found that stent or balloon intervention could lead to mild damages to the CW, especially in the PoSS.

Morphological findings

Many neurosurgeons have recently turned their attention to the CW, which was recognized by early anatomists. Schmutz broadly identified the morphological characteristics of the CW in the SSS and divided the CW into three different forms: valve-like lamellae, longitudinal lamellae, and trabeculae.[17] Valve-like lamellae represented the most common form, whereas longitudinal lamellae were the least common. Shao et al.[15] and Sharifi et al.[16] visualized and described the structural and topographical features of the CW with the aid of rigid endoscopy. They also identified three types of CW in all examined specimens. Similar to Schmutz, they also confirmed that CW were most commonly observed in the parietooccipital region and that its most common type was valve-like. In our study, we also observed three types of CW in the SS; we found that valve-like lamellae, which were located in the junction (between IW and lateral wall), were the most common type of CW in the SS.

The previous investigation identified the presence of septa in the SS and found they were located in either the straight section of the SS or the whole SS.[4] The differently shaped septa divided the SS into double or triple lumens.[18],[19],[20] In our study, the size of the septum, which was identified as a longitudinal chordae, was >2 mm. The longitudinal chordae were mostly detected at the anterior opening of the SS and extended into the confluence of sinuses.

Histology investigation of the chordae willisii

Throughout fetal development, the intraluminal structures in the dural sinuses likely come from the cells of the primitive veins in the epidural space, which merge to form different sized structures into venous sinuses. During the formation of the SS, dural folds form as the brain tissue is compressed between the mesencephalon and rhombencephalon.[21]

Accurate knowledge about the histological structure of the SS should be particularly beneficial to interventional neuroradiologists performing procedures inside the dural sinuses as this knowledge may significantly affect the difficulty and risk of the procedure. In the SS, the thicker IW compared with the lateral walls was due to the presence of larger amounts of tissues (including elastic fibers, connective tissue, blood vessels, and nerve fibers). The percentage of collagen fibers was lower in the posterior portion of the SS compared with the SSS or the TS. Moreover, transmission electron microscopy revealed the presence of muscle fibers in the IW of the SS, extending from its junction with the great cerebral vein to the confluence of sinuses.[11] The CW in posterior cranial fossa consists predominantly of collagen tissue and rarely contain endothelial lined vascular channels. The occurrence and thickness of the CW vary among different dura sinuses.[11] In our study, we found larger amounts of collagen fibers both in longitudinal lamellae and trabeculae.

Clinical significance on MMT studies

Interventional neuroradiology has to frequently use retrograde navigation through the main dural sinuses to treat arteriovenous malformations or fistulas, and sometimes, idiopathic chronic intracranial hypertension due to sinus thromboses or hypertrophic arachnoid granulations. The results of this study show that upon frequent usage of such types of procedures, minor iatrogenic damage to the lamellae and trabeculae may result in the exposure of collagen fibers in small areas. Clinically, intraoperative application of anticoagulant drugs reduces the chance of thrombosis. However, in rare cases, the balloon or the stent may cause severe damages to the CW, and therefore, increase the area of exposure of collagen fibers resulting in possible activation of blood coagulation. The existence of valve-like lamellae and longitudinal lamellae in the SS can cause the catheter to move into a blind cavity in the PoSS. A catheter could progress into the narrow channels surrounded by trabeculae and the sinus wall and cause the stent to open unsuccessfully. Therefore, understanding the detailed anatomy of the SS may help surgeons to avoid procedural difficulties and to achieve a higher success rate.

Limitations

We acknowledge that our study has some limitations. First, it does not provide guidance about how to avoid intraoperative damage to the intraluminal structures during transvenous endovascular therapy. However, knowledge of the internal structures of the SS, especially the distribution of the CW in different segments of the SS, provides a foundation for surgeons to navigate through technical problems. Second, it is uncertain which type of damage to the CW has a greater hemodynamic impact but it is very likely that the seriousness of the damages affects the risk of thrombosis.


 » Conclusion Top


With the aid of endoscopy, we described the distribution of intraluminal structures in the SS. We also demonstrated the minor damages to the CW caused by a stent or a balloon when they were navigated through the SS.

Informed consent

The consent of usage form was signed by the donor or the relatives of the donors who were all above age 18.

Ethics approval

Ethics approval was obtained from the ethics committee of Southern Medical University Zhujiang Hospital and Guangxi Medical University.

Financial support and sponsorship

This study received funding from the Science and Technology Project Foundation of Guangdong Province (grant no. 2015A030313259), the Clinical Research of Guangxi Autonomous Region (Z 20200158), and the Clinical Research of Liuzhou General Hospital. (grant no. LRY202015).

Conflicts of interest

There are no conflicts of interest.



 
 » References Top

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Choudhri O, Steinberg GK. Microsurgical treatment of a tentorial galenic dural arteriovenous fistula. Neurosurg Focus 2016;40(Video Suppl 1):2016.2011.FocusVid. 15420. doi: 10.3171/2016.1.FocusVid. 15420.  Back to cited text no. 2
    
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Taniguchi S, Harada K, Kajihara M, Fukuyama K. Combined use of stent-retriever and aspiration thrombectomy for cerebral venous sinus thrombosis involving the straight sinus: A case report. Interv Neuroradiol 2017;23:605-8.  Back to cited text no. 3
    
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Washida K, Kowa H, Tsuji Y, Sekiguchi K, Kanda F, Toda T. Multiple deep white matter hyperintense lesions on diffusion-weighted imaging: Early sign of straight sinus thrombosis. J Stroke Cerebrovasc Dis 2016;25:e131-3.  Back to cited text no. 4
    
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Ilyas A, Chen CJ, Raper DM, Ding D, Buell T, Mastorakos P, et al. Endovascular mechanical thrombectomy for cerebral venous sinus thrombosis: A systematic review. J Neurointerv Surg 2017;9:1086-92.  Back to cited text no. 7
    
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Browder J, Kaplan HA, Krieger AJ. Anatomical features of the straight sinus and its tributaries. J Neurosurg 1976;44:55-61.  Back to cited text no. 8
    
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Tsutsumi S, Ono H, Yasumoto Y. Cerebrospinal fluid spaces between intracranial venous sinuses and overlying dura mater: magnetic resonance imaging. Neuroradiol J 2018;31:177-81.  Back to cited text no. 10
    
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Amato MC, Tirapelli LF, Carlotti CG Jr, Colli BO. Straight sinus: Ultrastructural analysis aimed at surgical tumor resection. J Neurosurg 2016;125:494-507.  Back to cited text no. 11
    
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Dagain A, Vignes JR, Dulou R, Dutertre G, Delmas JM, Guerin J, et al. Junction between the great cerebral vein and the straight sinus: An anatomical, immunohistochemical, and ultrastructural study on 25 human brain cadaveric dissections. Clin Anat 2008;21:389-97.  Back to cited text no. 12
    
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Balik V, Uberall I, Sulla I, Ehrmann J, Kato Y, Sulla IJ, et al. Variability in wall thickness and related structures of major dural sinuses in posterior cranial fossa: A microscopic anatomical study and clinical implications. Oper Neurosurg (Hagerstown) 2019;17:88-96.  Back to cited text no. 13
    
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Balik V. Histological structure of the major dural sinus walls in the posterior cranial fossa: A factor that might matter in dural sinus surgery. World Neurosurg 2019;128:431-2.  Back to cited text no. 14
    
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Shao Y, Sun JL, Yang Y, Cui QK, Zhang QL. Endoscopic and microscopic anatomy of the superior sagittal sinus and torcular herophili. J Clin Neurosci 2009;16:421-4.  Back to cited text no. 15
    
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Sharifi M, Kunicki J, Krajewski P, Ciszek B. Endoscopic anatomy of the chordae willisii in the superior sagittal sinus. J Neurosurg 2004;101:832-5.  Back to cited text no. 16
    
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Schmutz HK. The chordae Willisii in the superior sagittal sinus: Morphology and classification. Acta Anat (Basel) 1980;108:94-7.  Back to cited text no. 17
    
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Kaplan HA, Browder J. Neurosurgical consideration of some features of the cerebral dural sinuses and their tributaries. Clin Neurosurg 1976;23:155-69.  Back to cited text no. 18
    
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Kedzia A, Kedzia W. Morphology of the Willis chords in the superior sagittal sinus during various periods of life. Folia Morphol (Warz) 2003;62:255-7.  Back to cited text no. 21
    


    Figures

  [Figure 1], [Figure 2], [Figure 3], [Figure 4]
 
 
    Tables

  [Table 1], [Table 2]



 

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