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Original research
Impaired drainage of vein of Labbé following venous sinus stenting for idiopathic intracranial hypertension
  1. Srikanth R Boddu1,2,
  2. Y Pierre Gobin1,
  3. Marc Dinkin3,
  4. Cristiano Oliveira3,
  5. Athos Patsalides1
  1. 1 Division of Interventional Neuroradiology, Department of Neurological Surgery, New York Presbyterian Hospital/Weill Cornell Medical Center, New York, USA
  2. 2 Interventional Neuroradiology, New York Presbyterian Queens Hospital, New York, USA
  3. 3 Department of Ophthalmology, New York Presbyterian Hospital, Weill Cornell Medical College, New York, USA
  1. Correspondence to Dr Athos Patsalides, Division of Interventional Neuroradiology, Department of Neurological Surgery New York Presbyterian Hospital/Weill Cornell Medical Center New York USA ; atp9002{at}med.cornell.edu

Abstract

Purpose The impact of venous sinus stenting (VSS) on vein of Labbé (VOL) drainage is poorly understood. The purpose of the study is to examine the incidence and potential high risk factors of impaired VOL drainage among idiopathic intracranial hypertension (IIH) patients following VSS.

Materials and methods Institutional review board approved prospective evaluation of all IIH patients who underwent VSS over a 5 year period (January 2012 to December 2017) at Weill Cornell Medical Center constituted the study population. Patient demographics, procedural details (laterality of stenting, balloon angioplasty, number of stents, and stent diameters), morphology of the VOL and changes in the flow in the VOL, type of sinus stenosis, and transverse sinus symmetry were evaluated. We used χ2 analysis to evaluate impaired VOL drainage against other variables. Statistical significance was set at 0.05.

Results 70 consecutive patients (67 women, 3 men) with a mean age of 31±9.8 years underwent VSS. Stenosis was extrinsic in 63% (n=44) and intrinsic in 37% (n=26) of patients. Impaired drainage of the VOL was detected in 9/70 (13%) patients. Ipsilateral VOL was recognized as dominant in 20% (n=14), co-dominant in 51% (n=36), and non-dominant in 29% (n=20) of patients. Impaired VOL drainage was significantly associated with ipsilateral VOL dominance (P=0.001) and stent diameter of ≥9 mm (P=0.042). All patients demonstrated widely patent VOL on follow-up contrast enhanced MR venography at 3 months and 24 months.

Conclusion Impaired drainage of the ipsilateral VOL is a potential consequence of VSS with 13% incidence, and has significant association with ipsilateral superficial cortical venous drainage via dominant VOL and stent diameter of ≥9 mm.

Clinical trial registration NCT01407809.

  • intracranial pressure
  • stenosis
  • vein
  • angiography
  • intervention

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Introduction

Venous sinus stenting (VSS) is gaining acceptance as an effective surgical treatment for selected patients with idiopathic intracranial hypertension (IIH) and venous sinus stenosis.1 In these patients, the stenosis most commonly occurs in the distal transverse and proximal sigmoid venous sinuses.2 3 The vein of Labbé (VOL) is the most important anastomotic vein of the temporal cortical venous system and usually drains into the distal transverse sinus or the transverse–sigmoid junction.4 Therefore, patients treated with VSS have stents placed across the transverse and sigmoid sinuses, covering the VOL ostium as it drains into the venous sinuses.5 6 This may have potentially severe consequences, such as cerebral edema, venous cerebral ischemia, and cerebral hemorrhage. The actual impact of venous sinus stenting on drainage of the VOL is not well understood, with conflicting evidence in the literature. Levitt et al5 reported no immediate occlusions of the VOL after VSS. In contradistinction, Raper et al6 reported abnormal findings in the VOL after VSS in 25% of patients immediately post-treatment and in 28% of patients at the 3 month follow-up (26% diminished caliber and 2% prolonged transit time).

The purpose of our study was to evaluate the incidence of impaired drainage of the VOL following VSS immediately, in the short term (3 months), and in the long term (24 months) after VSS, and identify anatomical and technical factors associated with this condition.

Materials and methods

Patient population

All patients with IIH who underwent treatment with VSS at Weill Cornell Medical center over a 5 year period (January 2012 to December 2017) constituted the study population. Institutional review board approval was obtained for data collection and analysis, and all data were collected prospectively. The VSS procedural details were described in prior publications from our group.1 7 All VSS procedures were performed by one physician (AP). Briefly, the VSS procedure requires dual antiplatelet therapy with aspirin and clopidogrel, initiated 1 week before the procedure and continuing for 1 month post-procedure, with continued aspirin monotherapy for 5 more months. A catheter venogram under local anesthesia was performed to obtain venous sinus pressure measurements through a microcatheter positioned in the superior sagittal, transverse, and sigmoid sinuses, and the jugular bulb. A trans-stenotic gradient ≥8 mm Hg was a prerequisite for stenting. Precise pro stent (Cordis) was used for all cases and stent placement was performed under general anesthesia. Angiography from the ipsilateral common carotid artery was performed immediately before and after placement of the stent while the patient was under general anesthesia, to assess arterial and venous flow in the ipsilateral hemisphere.

Data collection

All data were prospectively collected and included patient demographics, weight (kg), body mass index, procedural details (laterality of stenting, balloon angioplasty, number of stents, and stent diameters), morphology of the VOL and changes in the flow in the VOL, type of venous sinus stenosis, and transverse sinus symmetry.

Type of cerebral venous sinus stenosis

The type of venous sinus stenosis was documented with pretreatment MR venography (MRV) and catheter venography. Extrinsic stenosis was defined as a long segment stenosis with obtuse margins, whereas intrinsic stenosis was defined as a short segment stenosis with acute margins and a focal filling defect in the venous sinus lumen (figure 1).

Figure 1

Nature of stenosis. (A) Intrinsic stenosis—focal luminal narrowing (arrow). (B) Extrinsic stenosis— smooth long segment (arrows) narrowing.

Variability in VOL drainage

We categorized the morphology of VOL as dominant, co-dominant, and non-dominant based on the size of the VOL compared with the size of the superficial middle cerebral vein and the vein of Trolard, according to the classification of the superficial cerebral vein by Kawamata et al8 (figure 2).

Figure 2

Variability in vein of Labbé (VOL) drainage. (A) Dominant VOL (arrow) with hypoplastic vein of Trolard (arrowhead). The superficial middle cerebral vein (SMCV) is not seen. (B) Co-dominant VOL (arrow) along with the vein of Trolard (arrowhead) and faint SMCV (star). (C) Non-dominant VOL (arrow) with predominant drainage from the SMCV (star) and vein of Trolard (arrowhead).

Transverse sinus symmetry

The pattern of venous outflow from the superior sagittal sinus to the transverse sinuses was documented using pretreatment contrast enhanced MRV (CE-MRV). As reported in a previous publication from our group, a co-dominant system was considered when the transverse sinuses were symmetric with <3 mm difference in maximal diameter on CE-MRV.7 9 A unilateral dominant system was considered when there was absence of one transverse sinus (ie, aplastic) or asymmetric transverse sinuses with >3 mm difference in maximal diameter (hypoplastic).

Follow-up imaging

Follow-up CE-MRV at 3 and 24 months post VSS is part of our routine follow-up protocol. We used these studies to evaluate stent patency, patency of the VOL, and for the presence of new foci of signal abnormalities on ipsilateral temporo-parietal distribution. A catheter angiogram during the follow-up period was only performed if there was concern for treatment failure due to stenosis from new venous sinus stenosis. All scans were reviewed by two of the authors (SRB and AP) and the findings reported after consensus agreement.

Changes in flow in VOL

The immediate post-stent common carotid angiogram was used to classify VOL flow in comparison with the baseline pre-stent common carotid angiogram. We used a binary variable to characterize post-stenting flow in the VOL: normal flow or impaired flow. Normal flow means identical flow in the VOL in the ipsilateral common carotid artery runs before and after VSS. Impaired flow included any of the following: delayed flow in the VOL, reduced caliber of the VOL, or occlusion of the VOL (figures 3–5).

Figure 3

Normal drainage of the vein of Labbé (VOL) (A) Pre-stent: simultaneous opacification of the VOL along with other superficial cortical veins and dural venous sinuses. (B) Post-stent: simultaneous opacification of the VOL along with other superficial cortical veins. (C) Post-stent: note the washout of the VOL and other superficial cortical veins prior to the dural venous sinuses, a normal drainage pattern.

Figure 4

Impaired drainage of the vein of Labbé (VOL). (A) Pre-stent: simultaneous opacification of the dominant VOL (arrow) along with other superficial cortical veins and dural venous sinuses. (B) Post-stent: prolonged stasis/delayed drainage of the VOL (arrow) beyond the washout of other superficial cortical veins. (C) Post-stent: prolonged stasis/delayed drainage of the VOL (arrow) beyond the washout of the dural venous sinuses.

Figure 5

Impaired vein of Labbé (VOL). (A) Pre-stent angiogram with focal stenosis in the distal transverse sinus. (B) Post-stent angiogram with delayed drainage of the VOL (arrow). Note the improved luminal caliber of the transverse sinus stenosis.

Management of impaired flow

When impaired flow in the VOL was identified, the patients were maintained on a heparin drip for 24 hours (target activated partial thromboplastin time of 50–70 s) and then on anticoagulation for 2 weeks, in addition to the dual antiplatelet therapy. No additional imaging or procedures were performed in the group of patients with impaired flow in the VOL.

Statistical analysis

Statistical analysis was performed with Graphpad Prism 7 (Graph pad software, San Diego, California, USA). The outcome variable impaired drainage of the VOL was considered categorical. Among the dependent variables, age and body mass index were considered as continuous variables. The laterality of stenting, type of stenosis, transverse sinus drainage pattern, balloon angioplasty, drainage pattern of the ipsilateral VOL, number of stents used, and laterality of stenosis were considered as categorical variables. Both continuous and categorical evaluation was performed for number of stents deployed (single versus multiple stents) and stent diameters (≤8 mm vs ≥9 mm). Mean, range and SD were calculated for continuous variables. χ2 analysis was used to find the association between the outcome variable (impaired VOL drainage) and other categorical variables. The significance level for the analyses was 0.05.

Results

We report the results from 70 consecutive patients who underwent VSS at Weill Cornell Medical Center, 67 women and 3 men (age range 7–59 years, mean 31±9.8 years). Average weight and body mass index of the study cohort were 93±25.6 kg (range 30.8–144.2 kg) and 34.5±8.8 kg/m2 (range 16.4–51.4 kg/m2), respectively. Table 1 summarizes the demographics, procedural characteristics, anatomic details and follow-up of the nine patients with impaired VOL drainage.

Table 1

Summary of patients with impaired vein of Labbé drainage following venous sinus stenting for intracranial hypertension

Procedural characteristics

All patients had unilateral VSS, involving the right transverse and sigmoid sinuses in 51 (73%) and the left transverse and sigmoid sinuses in 19 (27%) patients. The average number of stents in our cohort was 1.5±0.6 (range 1–4). The majority of patients were treated with a single stent (64%; n=45) followed by 31% (n=22) with two overlapping stents. Two patients had three and a single patient had four overlapping stents. The median stent diameter was 8 mm (range 6–10mm). Balloon angioplasty was performed in 37% (n=26) of patients. The stent construct spanned across the VOL ostium in all cases. There were no neurological complications. Two patients developed small retroperitoneal hematomas from a femoral arterial puncture that were managed medically without the need for transfusion or surgery.

Type of stenosis, transverse venous sinus symmetry, and VOL dominance

The sinus stenosis was characterized as extrinsic in 63% (n=44) and intrinsic in 37% (n=26) of patients. A co-dominant transverse sinus drainage pattern was demonstrated in 40% (n=28) of patients and a unilateral dominant pattern was seen in 60% (n=42). Ipsilateral VOL was recognized as dominant in 20% (n=14), co-dominant in 51% (n=36) and non-dominant in 29% (n=20) of patients.

Impaired VOL drainage

Impaired drainage of the VOL was detected in 9/70 (13%) patients. All nine patients demonstrated diminished flow and caliber of the VOL. There was no instance of VOL occlusion. Among the nine patients with impaired VOL drainage, right transverse–sigmoid sinus stenting was noted in 7 (78%), extrinsic stenosis in 7 (78%), and unilateral dominant transverse sinus in 6 (67%). The angiographic pattern of VOL in this subset of patients was dominant in 6 (67%), co-dominant in 2 (22%), and non-dominant in 1 (11%). Seven (78%) had a single stent and two patients (22%) had multiple (two and four) stents. The median stent diameter in this subset was 9 mm (67%, n=6), followed by 8 mm (22%, n=2), and 10 mm (11% n=1). Balloon angioplasty was performed in 56% (n=5) of patients.

Statistical analysis

The χ2 analysis of outcome variable versus the studied parameters showed a significant association for impaired VOL drainage with dominance of ipsilateral VOL (P=0.001) and stent diameter of ≥9 mm (P=0.042). The laterality of stenting (P=0.869), type of stenosis (P=0.501), transverse sinus drainage pattern (P=0.762), number of stents (P=0.443), and balloon angioplasty (P=0.483) showed no statistically significant association with impaired VOL flow. Independent sample t test of the continuous variables, such as age (P=0.724), weight (P=0.881), and body mass index (P=0.612), showed no statistically significant variation between patients with and without impaired VOL drainage.

Follow-up evaluation

Follow-up CE-MRV at 3 months and 24 months post-stenting was available for all (n=70) and 39% (n=27) of patients, respectively. All patients with impaired VOL drainage (n=9) had 3 month follow-up imaging and 78% (n=7) had 2 year follow-up imaging. All patients demonstrated widely patent VOL on follow-up CE-MRV at the 3 month and 24 month follow-up imaging with similar VOL caliber compared with pretreatment CE-MRV. None of the patients with VOL impairment had parenchymal abnormalities in the temporo-parietal distribution, suggestive of venous ischemia or hemorrhage. Follow-up catheter angiography was performed in 11/70 patients and in 3/9 patients with impaired VOL flow. The VOL was patent with normal flow in all patients with follow-up angiogram Figure 6.

Figure 6

Follow-up of impaired vein of Labbé (VOL). (A, B) Pre-stent angiogram shows venous sinus stenosis and VOL (arrows). (C, D) Post-stent angiogram shows delayed flow and decreased caliber of the VOL (arrows) immediately after stenting (same projections as A and B). The patient was treated with anticoagulation for 2 weeks. (E, F) Follow-up MR venography shows a patent VOL (arrows) and patent transverse sinus stent. (G, H) Repeat angiogram at 1 year after VSS shows normal flow in the VOL.

Discussion

In this paper, we focused on the impact of VSS on ipsilateral drainage of the VOL, a potential source of serious adverse events related to VSS. Awareness regarding the incidence and pathophysiology of this condition is important to prevent procedural complications. In what is to our knowledge the largest series of VSS evaluating the impact on VOL drainage, we found an incidence of 13% for impaired drainage of the VOL after VSS. The post-stent impaired VOL drainage in all of our patients was detected immediately post-stent with angiography and was successfully treated with short term (14 days) anticoagulation in addition to the standard dual antiplatelet regimen.

The VOL typically connects the superficial middle cerebral vein to the transverse sinus8 and predominantly drains the lateral temporal lobe along with tributaries from the medial, anteroinferior, and posteroinferior temporal lobe in 80% of cadaveric dissections.10 The morphology and location of the vein itself is highly variable, with a dominant single channel or multiple branching channels or venous lakes, located along the mid-temporal (60%), posterior temporal (30%), and anterior temporal (10%).11 The sequelae of impaired venous drainage/thrombosis of the VOL may range from subclinical venous infarcts to cerebral edema, venous infarct, and hemorrhage of the ipsilateral temporal lobe,12 13 which is mainly affected by the collateral network and dominant venous drainage between the inferior anastomotic VOL versus the superior anastomotic vein of Trolard.

Mechanism of impairment of VOL flow

We believe there are two possible mechanisms of impaired flow in the VOL post VSS: (1) deformity of the venous sinus leading to increased pressure on the segment of the VOL as it traverses the wall of the venous sinus (dura) and changes in the orientation of the ostium on the wall of the venous sinus and (2) coverage/blockage of the ostium of the VOL by the stent struts.

The dural venous sinuses are enclosed between the periosteal and meningeal dural reflections. The superficial cortical veins traverse the cerebral surface in the subarachnoid space and drain into the dural venous sinuses either by directly piercing the meninges or indirectly via the meningeal veins with a variable subdural course.10 11 14 A recent microscopic anatomic study by Fang et al4 demonstrated that 20% of the VOL drain indirectly into the transverse sinuses through the meningeal veins. These meningeal veins have a flat configuration and run parallel to the sinus with an average subdural course of 10.0±7.2 mm, extending up to 23.6 mm in length. Our results showed a significantly increased risk of impaired VOL drainage with stent diameters of ≥9 mm. This finding is consistent with the notion that larger stent diameters are likely to cause more deformity of the transverse venous sinus, exert pressure on the segment of the VOL that runs parallel to the sinus, and thus impair drainage of the VOL. Over the years, we have modified our technique using smaller stents (≤8 mm) in order to decrease the risk of VOL impairment.

Coverage of the VOL ostium with the stent struts is another postulated mechanism for impaired VOL drainage, with an increased risk if the stents are overlapped across the ostium of the VOL. In our practice we often use overlapping stents to treat the entire transverse and sigmoid sinuses, but we avoid overlapping the stents across the ostium of the VOL after localizing it on pre-stent angiography. This explains why we did not have an increased incidence of impaired flow in the group of patients treated with multiple overlapping stents.

In our cohort, patients with superficial cortical venous drainage by a dominant VOL had a significantly higher association with impaired VOL drainage following VSS. It is tempting to speculate that in cases of superficial cortical venous system with dominant drainage via the superficial middle cerebral vein and/or the vein Trolard, alteration of flow dynamics of the VOL following VSS across its ostium is compensated by the collateral pathways. On the other hand, when the superficial cortical venous is primarily via the VOL (ie, dominant VOL pattern), any subtle flow alteration will be more conspicuous due to the paucity of collateral channels. The relatively uncommon incidence of impaired VOL flow following VSS can be partly attributed to such a low prevalence of the isolated dominance of the VOL, which was noted in 2.9% of cases in a cadaveric study of 266 cerebral hemispheres.8

In 2015, Levitt et al reported no effect on drainage of the VOL immediately after stenting in 35 IIH patients with stents placed across the ostium of the VOL (38 patients were reviewed). Similarly, there were no changes in flow in the VOL in 21 patients with long term angiographic follow-up over 35 months.5 Our results are clearly different. A possible explanation is that in this cohort of patients, a Zilver biliary self-expanding stent was used (Cook), as opposed to the Precise-Pro (Cordis) stent used in our patients.

In 2017, Raper et al6 reported a 25% incidence of impaired VOL flow immediately following VSS. The reported 25% incidence is based on 32 patients with post-stent arteriography, which constitutes only 57% of the cohort of patients with VSS, as the remaining 43% were lacking control arteriography following VSS. The majority of patients with impaired VOL flow had sluggish flow (19%) whereas the rest had diminished caliber (3%) or occlusion (3%). Of 46 patients with follow-up angiography, there was impaired VOL flow in 28%, the vast majority of which demonstrated diminished caliber (26%) and the rest sluggish flow (2%). The patient with occluded VOL immediately post-stenting actually improved with diminished caliber at follow-up angiography. In addition, one patient with sluggish flow post VSS developed VOL occlusion at follow-up. The authors did not treat impaired VOL flow with anticoagulation. There were no neurological sequalae. Our results differ from this study, as the incidence of VOL impairment in our series was lower. We used a different classification system from this group, but we did include the same variables (VOL flow, VOL size). There was no VOL occlusion in our cohort, either immediately or at follow-up. All of our patients had angiograms immediately post-stent but very few of our patients had angiograms during follow-up, which is more sensitive than CE-MRV in identifying subtle changes in VOL flow. CE-MRV is very sensitive however in showing occlusion of the VOL which is the main long term concern after initial impairment in flow.

Despite the lack of neurological adverse events in our study as well as in the study of Raper et al, the potential consequences of the impaired VOL going undetected should not underestimated. Lavoie et al reported a fatal cerebellar hemorrhage immediately after VSS, secondary to either the mechanical impairment of cerebellar venous drainage by the stent or venous perforation with guidewire.15 Buell et al reported a case of intracranial dural arteriovenous fistula (DAVF) after VSS in an IIH patient, a counterintuitive concept to the use of VSS to treat DAVF with preservation of the draining sinus.16 The authors postulated hemodynamic alterations secondary to VSS, subclinical cortical vein thrombosis despite dual antiplatelet therapy, vascular endothelial growth factor, and platelet derived growth factor stimulation from VSS induced inflammation in the pathogenesis of DAVF. A final check arterial angiogram following VSS helps in the early detection of flow alteration in the cortical veins.

Following confirmation of impaired VOL drainage on post-stent arteriography, we have empirically treated our patients with a heparin drip for 24 hours followed by anticoagulation for 2 weeks, in addition to a dual antiplatelet regimen. All patients had widely patent VOL on follow-up CE-MRV with no clinical or imaging evidence of venous edema or stroke. It is difficult to know the natural history of impaired VOL flow if the patients were treated with anticoagulation. It is reasonable to assume that when flow in the VOL is impaired, there is a risk of occlusion with probable clinical consequences. Anticoagulation will prevent acute thrombosis and occlusion and allow for formation of collateral flow if necessary. After the initial change in VOL flow, anticoagulation prevents thrombosis and allows time for the VOL to compensate and remain patent despite the decreased flow. Anticoagulation in addition to dual antiplatelet therapy carries an added risk of hemorrhagic complication, systemic, cerebral, or at the arterial puncture site, and is not a decision to be made without careful consideration of the pros and cons. In our opinion, the risks related to short term anticoagulation in this group of generally young and otherwise healthy patients outweigh the risks and we have used this approach for every patient with impaired VOL flow.

Limitations

There are several limitations to this study. Although the data were collected prospectively, the analysis is retrospective and subject to the inherent limitations of a retrospective study. An additional limitation is that the standard follow-up evaluation of our patients was with CEMRV, except in patients with clinical presentation suggestive of re-stenosis. Evaluation on CE-MRV is largely limited to the lumen patency and caliber without temporal information of flow pattern (ie, delayed drainage). However, we argue that persistently delayed drainage or prolonged stagnation in the VOL over 3 months without complete occlusion is unlikely. Despite all of our patients being on a dual antiplatelet regimen for 5–7 days prior to VSS, patients were not routinely tested for adequate platelet inhibition. Although none of our patients had stent thrombosis or in-stent stenosis, we were uncertain if suboptimal platelet inhibition resulted in VOL drainage impairment immediately after the VSS. Lastly, one physician performed all VSS at a single center and hence the results should be generalized with caution.

Conclusion

Impaired drainage of the ipsilateral VOL is a potential consequence of VSS seen in 13% of patients in our cohort. There was a significant association of this phenomenon with ipsilateral superficial cortical venous drainage via a dominant VOL and stent diameter of ≥9 mm. We recommend angiography immediately post-stenting for early detection of this entity. In our experience, short term treatment with anticoagulation when impaired flow in the VOL is identified was useful to maintain patency and prevent neurological sequelae. Meticulous technique, selection of optimal stent length and diameter, and avoiding stent overlapping over the VOL ostium in multi-stent construct are vital in minimizing the incidence of impaired VOL drainage after VSS.

References

Footnotes

  • Contributors Conception of the work: AP and MD. Acquisition of the data: AP and SRB. Analysis and interpretation of the data and drafting the work: AP and SRB. Edited the manuscript for intellectual content: all authors. Revising the manuscript critically for important intellectual content, final approval of the version to be published, and agreement to be accountable for all aspects of the work in ensuring that questions related to the accuracy or integrity of any part of the work are appropriately investigated and resolved: all authors.

  • Funding The authors have not declared a specific grant for this research from any funding agency in the public, commercial, or not-for-profit sectors.

  • Competing interests YPG is the CEO and Medical Director and owns stocks in Serenity Medical Inc. SRB owns stocks in Serenity Medical Inc.MD has consulted for Serenity Medical Inc.

  • Patient consent Not required.

  • Ethics approval The study was approved by the institutional review board of Weill Cornell.

  • Provenance and peer review Not commissioned; externally peer reviewed.

  • Data sharing statement No additional data available.