A new transvenous approach to the carotid …...into the cortical veins (the SMCV and DMCV), SOV, and IOV (Fig. 1A). Initially, transarterial embolization of the inflowing ECAs was

J Neurosurg / Volume 116 / March 2012

J Neurosurg 116:581–587, 2012

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The transvenous approach via the IPS is the first es-tablished and most commonly used endovascular surgical method for CCFs2,5,18 and venous hor mone

sampling.9,16 However, the IPS route is not usually avail-able and when it is obstructed or anomalous through com-munication to the IJV, other venous drainage routes—such as through the superior petrosal sinus,12 the intercavern-ous sinus via the contralateral cavernous sinus,6 and the SOV—may be attempted.1,4,8,10 When the SOV is the sole drainage route except for cortical venous drainage, it often shows dilation. However, peripheral tributaries (roots) do not show a remarkable enlargement and often exhibit tor-tuous running and focal narrowing. Advancement of the

catheter may fail. We have ex perienced 3 cases of dural CCFs and 1 case of Cushing disease in which the conven-tional IPS approach proved impossible but which could be successfully accessed via the IPOV (Table 1). The ef-ficacy and safety of this access route in such difficult cases is discussed in this paper.

MethodsSince 1992, we have treated 76 patients with dural

CCFs using endovascular surgery. The most recent 18 pa-tients underwent transvenous embolization in addition to transarterial embolization. In 3 of these 18 patients, a con-ventional venous approach via the IPS failed. One dural CCF had only cortical venous drainage, another mainly drained into the same cortical veins but with slight inflow into the SOV and IOV, and the remaining CCF mainly drained into the SOV, IOV, and IPOV. During this period, a further 5 patients with Cushing syndrome underwent

A new transvenous approach to the carotid-cavernous sinus via the inferior petrooccipital vein

Clinical articleAkirA kurAtA, M.D.,1 SAchio Suzuki, M.D.,1 kAzuhiSA iwAMoto, M.D.,1 kuniAki nAkAhArA, M.D.,1 MADokA inukAi, M.D.,1 June niki, M.D.,1 kiMitoShi SAtou, M.D.,1 MASAru YAMADA, M.D.,1 kiYotAkA FuJii, M.D.,1 Shinichi kAn, M.D.,2 AnD toShiro kAtSutA, M.D.3

Departments of 1Neurosurgery and 2Radiology, Kitasato University School of Medicine, Kanagawa; and 3Department of Neurosurgery, Kitakyushu Municipal Medical Center, Fukuoka, Japan

Object. The transvenous approach via the inferior petrosal sinus (IPS) is commonly used as the most appropriate for carotid-cavernous fistula (CCF) or cavernous sinus sampling. However, sometimes the IPS is not accessible be-cause of anatomical problems and/or complications, therefore an alternative route is needed. In this paper, the authors present and discuss the utility of a transvenous approach to the cavernous sinus via the inferior petrooccipital vein.

Methods. Four patients, 3 with dural CCFs and the other with Cushing disease, in whom endovascular surgical attempts failed using a conventional venous approach via the IPS, underwent a transvenous approach to the cavernous sinus via the inferior petrooccipital vein (IPOV). One dural CCF case had only cortical venous drainage, the second CCF also mainly drained into the cortical vein with slight inflow into the superior ophthalmic vein and inferior oph-thalmic vein, and the third demonstrated drainage into the superior and inferior ophthalmic veins and IPOV.

Results. In all cases, the cavernous sinus could be accessed successfully via this route and without complications.Conclusions. The transvenous approach to the cavernous sinus via the IPOV should be considered as an alter-

native in cases when use of the IPS is precluded by an anatomical problem and there are no other suitable venous approach routes. (DOI: 10.3171/2011.4.JNS102155)

keY worDS • carotid-cavernous fistula • transvenous approach • endovascular surgery • inferior petrooccipital vein • pituitary surgery • interventional neurosurgery • surgical technique

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Abbreviations used in this paper: CCF = carotid-cavernous fistula; DMCV = deep middle cerebral vein; ECA = external carotid artery; IJV = internal jugular vein; IOV = inferior ophthalmic vein; IPOV = inferior petrooccipital vein; IPS = inferior petrosal sinus; SMCV = superficial middle cerebral vein; SOV = superior ophthalmic vein.

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superselective hormone sampling from the cavernous si-nus. In 1 of these 5 patients, the conventional transvenous approach via the IPS failed. For these 4 total patients (Ta-ble 1), the transvenous approach to the cavernous sinus via the IPOV was attempted.

Preoperatively, the activated coagulation time was assessed through a 5 Fr femoral arterial sheath under local anesthesia, followed by a bolus injection of 2000 units of heparin. During endovascular surgery, heparin was continuously infused to maintain activated coagula-tion time at 2–3 times the control value. A 5 Fr catheter (Envoy, Cordis/Johnson & Johnson) was placed in the af-fected carotid artery for repeated angiography and road mapping during endovascular surgery. A 6 Fr sheath was inserted into the contralateral site of the femoral vein. A 6 Fr catheter (Envoy, Cordis/Johnson & Johnson) was in-serted via the sheath and placed in the affected site of the jugular vein. Initially, a conventional angiogram from the femoral artery was obtained to make a road map in the venous phase. A 6 Fr catheter placed in the jugular valve was rotated in the anteromedial direction, followed by advancement of the microcatheter (Excelsior, Stryker) preceded by a microguidewire (Agility 10, Cordis/John-son & Johnson; or Transcent 10, Boston Scientific) into the cavernous sinus. With all 4 cases the transvenous approach via the IPS was initially attempted but failed. Next, the microguidewire was advanced slightly medial to the IPS route and the microcatheter was gently ad-vanced, preceded by the microguidewire. After the mi-crocatheter was placed in the affected cavernous sinus, its tip was defined by venography and advanced into a suitable position to stop the cortical venous drainage in patients with CCFs or the center of the cavernous sinus in the case with Cushing disease, followed by platinum coil embolization or venous sampling.

ResultsTwo of 3 cases with dural CCFs demonstrated main

inflow into cortical veins and the affected cavernous sinus could be successfully accessed via the IPOV and com-pletely occluded without complications. One patient with a dural CCF and inflow into the SOV, IOV, and IPOV also underwent transvenous embolization through the IPOV route and complete occlusion was established. Similarly, with the Cushing disease case, access to the cavernous

sinus via the IPOV proved possible and venous sampling was successfully performed without complications.

Case 1This 72-year-old man suddenly developed diplopia,

and was followed up conservatively in an outpatient clin-ic because the symptoms caused by left cranial nerve III palsy gradually improved with time. Six months later, the diplopia disappeared. However, left pulsating exophthal-mos, conjunctival chemosis, and pulsatile tinnitus devel-oped after 1 year. The patient was examined using MR imaging at another hospital and was referred to our in-stitution. Magnetic resonance angiography showed an in-crease of the vascular structure in the left cavernous sinus communicating with a dilated cortical vein. Angiography showed a dural CCF in the left cavernous sinus draining into the cortical veins (the SMCV and DMCV), SOV, and IOV (Fig. 1A). Initially, transarterial embolization of the inflowing ECAs was performed to decrease the inflowing arterial flow. Next, the transvenous approach via the IPS was tried, but this approach failed because of an obstruc-tion. The peripheral roots of SOV and IOV showed lack of dilation. The left IPOV route was then attempted (Fig. 1B and C), which proved successful without any com-plications. Angiography after the endovascular surgery showed no residual fistula and no cortical venous drain-age (Fig. 1D and E). Although left cranial nerve VI palsy developed 2 days later, this disappeared 3 months after the treatment. Follow-up MR angiography showed no re-currence of the CCF.

Case 2This 76-year-old woman suddenly developed diplo-

pia and she was followed-up conservatively in an outpa-tient clinic because her symptoms caused by left cranial nerve VI palsy gradually improved with time. Six months later, the diplopia disappeared. However, after 2 years, the patient developed symptoms and was examined using MR imaging at another hospital and referred to our in-stitution. Magnetic resonance angiography showed an in-crease of the vascular structure in the left cavernous sinus communicating with a dilated cortical vein. Angiography showed a dural CCF in the left cavernous sinus draining into the SMCV and DMCV only (Fig. 2A and B). Ini-tially, transarterial embolization of the inflowing ECAs was performed to decrease the inflowing arterial flow.

TABLE 1: Summary of 4 cases with a successful transvenous approach to the cavernous sinus via the IPOV*

Case No.

Age (yrs), Sex Initial Sx (Disease) Venous Drainages Purpose Treatments Outcome FU (mos)

1 72, M diplopia (dural CCF) SMCV, DMCV, SOV, IOV

TVE TAE & TVE cure 4

2 76, F diplopia (dural CCF) SMCV, DMCV TVE TAE & TVE cure 13 77, F lt chemosis (dural CCF) IPOV, SOV, IOV TVE TAE & TVE cure 104 67, F moon face (Cushing) none venous sampling surgical removal complete re-

moval 2

* There were no complications in any of the cases. Abbreviations: FU = follow-up; TAE = transarterial embolization; TVE = trans-venous embolization.


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Next, the transvenous approach via the IPS was tried, but this failed because of an obstruction of the IPS. The left IPOV route was then attempted (Fig. 2C), and this proved successful without any complications. Angiography after the endovascular surgery showed no residual fistula and no cortical venous drainage (Fig. 2D). Although, the left cranial nerve VI palsy worsened 2 days later, this disap-peared 3 months after the treatment. Follow-up MR angi-ography showed no recurrence of the CCF.

Case 3This 77-year-old woman developed left chemosis,

and she was followed-up conservatively in an outpatient clinic. The symptoms worsened with time and proptosis also appeared. One month later, the patient was examined

using MR imaging at another hospital and was referred to our institution. Magnetic resonance angiography showed an increase of the vascular structure in the left cavern-ous sinus. Angiography showed a dural CCF in the left cavernous sinus draining into the SOV, IOV, and IPOV (Fig. 3A and B). Initially, transarterial embolization of the inflowing ECAs was performed to decrease the inflowing arterial flow. Next, the transvenous approach via the left IPOV route was then attempted (Fig. 3C and D), and this proved successful without any complications. Angiogra-phy after the endovascular surgery showed no residual fistula and no cortical venous drainage (Fig. 3E). Three months after treatment, the symptoms had completely disappeared and follow-up MR angiography showed no recurrence of the CCF.

Fig. 1. Case 1. Left carotid angiogram, lateral view (A), showing a CCF with drainage into the SMCV (double arrows), the DMCV (single arrow), SOV, and IOV. The peripheral roots of the SOV and IOV lack any dilation. Digital subtraction angiography, anteroposterior view (B), and skull radio-graph, anteroposterior view (C), showing venography from the microcath-eter into the left cavernous sinus via the IPOV (4 arrows). SMCV = double arrows, DMCV = single arrow. Left carotid angiogram, anteroposterior (D) and lateral (E) views, after endovascular surgery showing complete obliteration of the fistula and no cortical venous reflux.

Fig. 2. Case 2. Left carotid angiogram, anteroposterior (A) and lateral (B) views, showing a CCF with drainage limited to the SMCV (double arrows) and DMCV (single arrow). Skull radiograph, anteroposterior view (C), showing venography from the mi-crocatheter into the left cavernous sinus via the IPOV (arrows). Left ECA angiogram, anteroposterior view (D), after endovascular surgery showing complete obliteration of the fistula and no cortical venous refluxes.

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Case 4This 67-year-old woman was referred to our depart-

ment for cavernous venous sampling to distinguish be-tween Cushing disease and ectopic adrenocorticotrophic hormone syndrome. The patient showed no suppression by means of a high-dose dexamethasone suppression test (Liddle test), but a micropituitary adenoma was suspected on MR imaging. A transvenous approach to the right cav-ernous sinus via the right IPS was initially attempted, but failed because of an obstruction of the IPS. Next, the right IPOV route was attempted, which was successful. The left transvenous approach to the left cavernous sinus via the left IPS was conventionally performed (Fig. 4). Ve-nous sampling from the bilateral cavernous sinuses and femoral veins was possible and resulted in a diagnosis of Cushing disease caused by a micropituitary adenoma in the left side of the pituitary gland, which was successfully removed by a transsphenoidal approach.

DiscussionThe transvenous approach via the IPS2,5,18 for dural

CCF and hormone sampling16 from the cavernous sinus is the standard access route. However, when there is ob-struction of the IPS or other problem such as noncom-munication with the IJV, other venous drainage routes should be attempted. Benndorf et al.2 stated that a throm-bosed IPS may also become an alternative transvenous approach route for dural CCFs, reporting 4 cases and a re-view of the literature. Obstructions caused by secondarily formed thrombi that are not organized and not of great age may allow introduction of a microcatheter preceded by a guidewire.

However, when the obstruction of the IPS is stiff with an organized old thrombus,13 the other access route to the cavernous sinus is needed. In the present series, in 2 (11%) of 18 patients with dural CCFs (Cases 1 and 2) the conventional venous approach via the IPS failed. These 2 patients were referred to our institute more than 1 year after development of initial symptoms, which may have contributed to obstruction of the IPS with an orga-nized old thrombus. In Case 2 with only cortical venous drainage, another suitable access route other than the IPS was not present. In Case 1, the SOV was another drainage route, but the SOV and IOV did not show an adequate dilation; peripheral tributaries (roots) did not show any

Fig. 3. Case 3. Left carotid angiogram, anteroposterior (A) and lateral (B) views, showing a CCF with drainage into the SOV, IOV, and IPOV (4 arrows). Skull radiograph, anteroposterior (C) and lateral (D) views, showing the microcatheter with microgu-idewire introduced into the left cavernous sinus via the IPOV (4 arrows). Left carotid angiogram, anteroposterior view (E), after endovascular surgery showing complete obliteration of the fistula and no cortical venous reflux.



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enlargement, suggesting that the SOV was not a feasible access route.

In Case 3, the IPOV developed as the main venous drainage route for a dural CCF, which showed a new ap-propriate access route to the cavernous sinus. In Case 4 with Cushing disease, the right IPS was not in communi-cation with the IJV, as defined by venography of the right cavernous sinus (Fig. 4A).

Anatomy and Variation in the IPS and IPOVThe IPS is a dural sinus that extends from the poste-

rior aspect of the cavernous sinus 23–28 mm laterally and posteriorly to the IJV. It courses just lateral to the clivus, along the posterior inferior edge of the petrous ridge. It usually leaves the cranial cavity through the jugular fora-men, in an opening separated from the rest of the foramen by the anterior petrooccipital ligament.9 As it enters the jugular foramen, the IPS become a vein, approximately 2 mm in diameter, and enters the anteromedial aspect of the jugular bulb approximately 6 mm inferior to the level of its entrance to the jugular foramen.3 Shiu et al.15 described 4 types of variations of the junction between the IPS and the IJV, on the basis of their experience with cavernous sinus venography. In Type I, the IPS anastomosis with the IJV and the anterior condylar vein is small or absent (45%). In Type II, the anterior condylar vein is large and there is a prominent anastomosis of this vessel with the IPS (24%). In Type III, the IPS exists as several small channels, which may form a plexus. In Type IV, the IPS does not join the IJV, emptying directly into the anterior condylar vein (7%). Mitsuhashi et al.11 evaluated morpho-logical aspects of the caudal end of the IPS using 3D rota-tional venography. They described IPS drainage into the jugular bulb in only 1 (1.2%) of 83 sides, the remainder draining into the IJV below the jugular bulb. The IPS was found to drain directly into the vertebral plexus with no connection to the IJV in 3 (3.6%) of 83 sides and the IPS was absent in 14 (16.9%) of 83 sides. In this series, the IPS with no connection to the IJV was 1 (10%) of 10 found during venous sampling in the bilateral cavernous sinus in 5 patients.

Trolard17 initially named a small vein different from IPS as the IPOV. San Millán Ruíz et al.14 reported the

venous plexus of Rektorzik, corresponding to Trolard’s IPOV found coursing extracranially along the petrooc-cipital suture, which regularly contributed in forming the anterior condylar confluent.

Katsuta et al.7 called the IPOV the inferior petro-clival vein and stressed its utility: a small vein running in the extracranial groove (Fig. 5) of the petrooccipital fissure, flowing into the petrosal confluens (anterior con-dylar confluent) and acting like a mirror image of the IPS (Fig. 6). They reported that, although it is small, it may be dilated by high venous pressure in dural arteriovenous fistula cases, making it a useful route to introduce an in-travenous catheter into the cavernous sinus. This proved to be case in all of our present series of patients. To our knowledge there have been no previous reports of its use

Fig. 4. Case 4. Venography, anteroposterior view (A), from a microcather in the right cavernous sinus. IPS = single arrow (left and right), IPOV = 4 arrows, tip of the microcatheters = asterisk, obstruction of the right IPS = double asterisks. Skull radiograph, anteroposterior (B) and lateral (C) views, showing a microcatheter introduced into the left cavernous sinus via the left IPS (single arrow) and a microcatheter introduced into the right cavernous sinus via the IPOV (4 arrows).

Fig. 5. Photograph showing the IPOV running in the extracranial groove of the petrooccipital fissure.

A. Kurata et al.


as an actual access route to the cavernous sinus through the IPOV. The IPOV might be mistaken as the IPS be-cause their running courses resemble each other.

Techniques to Navigate the Microcather Into the Cavernous Sinus Through the IPOV

To navigate a small-diameter and soft-tip microcath-er into the IPOV, use of a preceding small soft guidewire is essential because it is a small vein,17 even if it is dilated. The microcatheter should be advanced taking into con-sideration the running course of the IPOV. Initially the IPOV origin from the medial part of the petrosal conflu-ence runs comparatively sharply medial to the IPS, and thereafter runs parallel and slightly deep with the IPS (mirror image), and finally changes to a lateral course as shown in the present series.

ConclusionsIn the event the IPS is unavailable as an access route

in patients with dural CCFs and in cases requiring hor-mone sampling, and other transvenous approaches are not available, our original IPOV approach to the cavernous sinus can be considered safe and reliable.

Disclosure

The authors report no conflict of interest concerning the mate-rials or methods used in this study or the findings specified in this paper.

Author contributions to the study and manuscript preparation include the following. Conception and design: Kurata. Acquisition of data: Kurata, Suzuki, Satou. Analysis and interpretation of data:

Kurata, Iwamoto, Nakahara. Drafting the article: Kurata, Inukai. Critically revising the article: Kurata, Niki, Yamada. Statistical analysis: Kurata, Fujii. Study supervision: Kan, Katsuta.

Acknowledgment

The authors thank Dr. Malcolm Moore for editing the manu-script.

References

1. Agid R, Willinsky RA, Haw C, Souza MPS, Vanek IJ, ter-Brugge KG: Targeted compartmental embolization of cavern-ous sinus dural arteriovenous fistulae using transfemoral me-dial and lateral facial vein approaches. Neuroradiology 46: 156–160, 2004

2. Benndorf G, Bender A, Lehmann R, Lanksch W: Transvenous occlusion of dural cavernous sinus fistulas through the throm-bosed inferior petrosal sinus: report of four cases and review of the literature. Surg Neurol 54:42–54, 2000

3. Bošković M, Savić V, Josifov J: Über die Sinus Petrosi und ihre Zuflüsse. Gengenbaurs Morphol Jahrb 104:420–429, 1963

4. Cheng KM, Chan CM, Cheug YL: Transvenous embolisation of dural carotid-cavernous fistulas by multiple venous routes: a series of 27 cases. Acta Neurochir (Wien) 145:17–29, 2003

5. Halbach VV, Higashida RT, Hieshima GB, Hardin CW, Yang PJ: Transvenous embolization of direct carotid cavernous fis-tulas. AJNR Am J Neuroradiol 9:741–747, 1988

6. Jahan R, Gobin YP, Glenn B, Duckwiler GR, Viñuela F: Transvenous embolization of a dural arteriovenous fistula of the cavernous sinus through the contralateral pteriogoid plex-us. Neuroradiology 40:189–193, 1998

7. Katsuta T, Matsushima T, Uda K: [Surgical anatomy of the skullbase venous system: petroclival region.] No Shinkei Ge-ka 17:738–744, 2008 (Jpn)

Fig. 6. Schematic drawing of the IPOV by T. Katsuta. v. = vein



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8. Lee JW, Kim DJ, Jung JY, Kim SH, Huh SK, Suh SH, et al: Embolisation of indirect carotid-cavernous sinus dural arte-rio-venous fistulae using the direct superior ophthalmic vein approach. Acta Neurochir (Wien) 150:557–561, 2008

9. Miller DL, Doppman JL: Petrosal sinus sampling: technique and rationale. Radiology 178:37–47, 1991

10. Miller NR, Monsein LH, Debrun GM, Tamargo RJ, Nauta HJW: Treatment of carotid-cavernous sinus fistulas using a superior ophthalmic vein approach. J Neurosurg 83:838–842, 1995

11. Mitsuhashi Y, Nishio A, Kawahara S, Ichinose T, Yamauchi S, Naruse H, et al: Morphologic evaluation of the caudal end of the inferior petrosal sinus using 3D rotational venography. AJNR Am J Neuroradiol 28:1179–1184, 2007

12. Mounayer C, Piotin M, Spelle L, Moret J: Superior petrosal sinus catheterization for transvenous embolization of a dural carotid cavernous sinus fistula. AJNR Am J Neuroradiol 23: 1153–1155, 2002

13. Oishi H, Arai H, Sato K, Iizuka Y: Complications associated with transvenous embolisation of cavernous dural arteriove-nous fistula. Acta Neurochir (Wien) 141:1265–1271, 1999

14. San Millán Ruíz D, Gailloud P, Rüfenacht DA, Delavelle J, Henry F, Fasel JH: The craniocervical venous system in rela-tion to cerebral venous drainage. AJNR Am J Neuroradiol 23:1500–1508, 2002

15. Shiu PC, Hanafee WN, Wilson GH, Rand RW: Cavernous si-nus venography. Am J Roentgenol Radium Ther Nucl Med 104:57–62, 1968

16. Teramoto A, Yoshida Y, Sanno N, Nemoto S: Cavernous si-nus sampling in patients with adrenocorticotrophic hormone-dependent Cushing’s syndrome with emphasis on inter- and intracavernous adrenocorticotrophic hormone gradients. J Neurosurg 89:762–768, 1998

17. Trolard P: Anatomie du système veineux de l’encéphale et du crane. Paris: Thèse de la Faculté de Médecine de Paris, 1868, pp 1–32

18. Yamashita K, Taki W, Nishi S, Sadato A, Nakahara I, Kiku-chi H, et al: Transvenous embolization of dural caroticocav-ernous fistulae: technical considerations. Neuroradiology 35:475–479, 1993

Manuscript submitted January 6, 2011.Accepted April 25, 2011.Please include this information when citing this paper: published

online June 17, 2011; DOI: 10.3171/2011.4.JNS102155.Address correspondence to: Akira Kurata, M.D., Department

of Neurosurgery, Kitasato University School of Medicine, 1-15-1 Kitasato, Minamik Sagamihara, Kanagawa 228-8555, Japan. email: [email protected].

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A new transvenous approach to the carotid …...into the cortical veins (the SMCV and DMCV), SOV, and IOV (Fig. 1A). Initially, transarterial embolization of the inflowing ECAs was