Abstract

Background: Parent artery occlusion (PAO) with or without bypass surgery is a feasible treatment for large intracavernous carotid artery (ICCA) aneurysms. The ideal occlusion site (internal or common carotid artery [CCA]) and ischemic complications after PAO have received special attention since the description of the technique. Unfrequently, some patients can also develop unusual external carotid artery-internal carotid artery collateral pathways distal to the ligation site that can explain the failure to aneurysm size reduction.

Case Description: We describe a rare case of delayed refilling of a large ICCA aneurysm partially thrombosed which early recanalized after surgical ligation of the cervical CCA through an unusual collateral pathway.

Conclusion: Based on our experience, we recommend periodic long-term follow-up neuroimaging, especially in those cases where potential collateral branches have not been clearly identified in the preoperative studies.

Keywords: Aneurysm, Collateral pathways, Intracavernous carotid artery, Parent artery occlusion

INTRODUCTION

Intracavernous carotid artery (ICCA) aneurysms account for 3–5% of all intracranial aneurysms.[ 35 ] Due to its location, the risk of mortality and severe morbidity in case of aneurysm rupture is low[ 42 ] and spontaneous thrombosis of the aneurysm has been reported.[ 21 ] For that reason, any proposed treatment has to have lower risk of complications than their natural benign history.[ 20 ] In general, aneurysms with extension to the subarachnoid space, erosion of the sphenoid bone, evidence of enlargement, or progressive symptomatic cases should be treated due to the risk of ophthalmoplegia, orbital pain, visual acuity decline, SAH, carotid-cavernous fistula, or thromboembolic events.[ 22 ]

In most centers, due to the challenging exposition of ICCA, these aneurysms are considered not amenable for clipping, and their management usually consists in coiling or flow-diverter placement. Parent artery occlusion (PAO) is a feasible alternative in those cases with intra-aneurysm or internal carotid artery (ICA) thrombosis, none or very wide neck, age or medical condition of the patient, and after failure of endovascular techniques. There are a number of alternatives according to the location (ICA or common carotid artery [CCA]), timing (abrupt ligation or prolonged closure with temporal clamps),[ 24 , 29 ] and the method for occlusion (surgical ligation[ 13 , 18 ] or endovascular procedures).[ 9 , 34 , 36 , 39 ] In addition, in those patients with moderate to high risk of ischemic complications, PAO should be preceded by revascularization techniques.[ 15 , 16 , 23 ]

The reported mortality and morbidity rates of surgical PAO range from 6–20% to 4–12%, respectively.[ 28 , 29 , 33 ] The main causes of worsening or death after PAO are cerebral ischemia, thromboembolism, intracerebral hemorrhage, and de novo or enlargement of contralateral brain aneurysms.[ 3 , 12 ] On the other hand, refilling of the ICCA aneurysm is a complication unfrequently reported after PAO.

Here, we present a rare case of a partially thrombosed ICCA aneurysm which early recanalized after surgical ligation of the cervical CCA via an unusual collateral pathway.

CASE REPORT

A 63-year-old woman, with arterial hypertension as the only relevant medical history, presented with a sudden binocular diplopia. Right 6^th nerve palsy was evidenced on physical examination at admission. AngioCT revealed a right ICCA aneurysm with signs of partial thrombosis without evidence of rupture [ Figure 1a ]. Patient’s symptoms worsened to complete cavernous syndrome 5-days later, and a new AngioCT showed progression of the thrombosis with discrete mass effect [ Figure 1b ], so steroids and antiplatelet therapy were initiated. Angiography on admission confirmed the presence of a giant aneurysm of the anterior portion of the right ICCA [ Figure 2a - c ]. Since endovascular techniques seemed inappropriate due to the partially intraluminal thrombosis and very wide neck, PAO was considered as the optimal treatment choice. A balloon test occlusion (BTO) was performed to evaluate the preoperative risk of ischemia without relevant findings and no evidence of retrograde filling of the aneurysm by anterior or posterior communicating arteries [ Figure 2d and e ]. Then, the patient underwent surgical ligation of the cervical CCA at the level of C6 with a 3/0-silk, and anticoagulation was started 3 days after surgery. Symptoms of cavernous sinus syndrome resolved with the exception of 6^th nerve palsy during postoperative recovery. A cerebral magnetic resonance angiography (MRA) revealed decrease of the size of the aneurysm lumen and no ischemic lesions were detected [ Figure 3a ].

Figure 1:

Admission AngioCT revealed a right intracavernous carotid artery (ICCA) aneurysm with signs of partial thrombosis without evidence of rupture (a). The patient experienced complete cavernous sinus syndrome in relation to progression of thrombosis of the ICCA aneurysm as a new AngioCT showed (b).

Figure 2:

Right carotid angiography, anteroposterior (a) lateral (b) and oblique (c) projections, indicates a giant aneurysm (25 mm of main diameter, 9 mm neck width) at the cavernous segment of the right ICA. Left carotid angiography, anteroposterior projection, showing adequate collateral reserve via anterior communicating artery (d) and the aneurysm without filling of contrast after balloon occlusion at the proximal portion of the right ICA (e).

Figure 3:

AngioMR (3D time of flight magnetic resonance sequence) showing reduction of the aneurysm size and minimal residual filling of the aneurysm immediately after the procedure (a). Eight months after the common carotid artery ligation, new AngioMR revealed signs of aneurysm recanalization (b).

Nine months later, and without new neurological symptoms, signs of aneurysm growth were detected in a serial MRA [ Figure 3b ], and a new angiography was planned. Right CCA angiogram showed the therapeutic occlusion of the right ICA, but the right vertebral angiogram demonstrated proximal partial recanalization of the ICCA aneurysm. Collateral supply was explained from the external carotid artery (ECA) through the occipital artery with an inverse flow to the ICA [ Figure 4a ]. Therefore, surgical occlusion of the cervical ICA at the level of the ansa cervicalis of the hypoglossal nerve with a 0-silk was performed, and intraoperative Doppler ultrasound revealed no efferent flow in ICA. Postoperative new angiography confirmed the total occlusion of the aneurysm [ Figure 4b ]. After 6 years of follow-up, we have not detected refilling or thromboembolic events [ Figure 5 ].

Figure 4:

Nine months after common carotid artery ligation, a right vertebral angiography (lateral projection) showed partial recanalization of the intracavernous carotid artery (ICCA) aneurysm (a). Collateral supply was explained from external carotid artery through the occipital artery with an inverse flow to the internal carotid artery (ICA) (arrowheads). After cervical ICA surgical ligation, a new right vertebral angiography confirmed total occlusion of the ICCA aneurysm (b).

Figure 5:

Last follow-up AngioMR showing the absence of flow in the right intracavernous carotid artery (a, 3D time of flight magnetic resonance sequence) and no evidences of ischemic lesions (b, diffusion-weighted imaging sequence).

DISCUSSION

In ICCA aneurysms, due to the small number and caliber of branching vessels, PAO is a feasible option for treatment.[ 7 ] The occlusion can be achieved by surgical ligation or by endovascular means. The treatment alternatives for symptomatic ICCA aneurysms with preservation of the parent artery include the obliteration of the aneurysm sac with coils[ 15 ] or flow diversion. There are evidences suggesting that coiling can be conducted with a low complication rate but the rate of recurrence is higher compared with PAO.[ 38 - 40 ] New generation of flow-diverters stents has shown encouraging results but the safety due to frequent technical complications (vasospasm, incomplete opening, and inability to place the flow-diverter due to vessel tortuosity) and long-term effectiveness is unknown.[ 31 , 32 ] In our patient, we selected the surgical ligation because the selective occlusion of the proximal arterial lumen with coils has been associated with higher rate of recanalization.[ 26 ] We also excluded aneurysm coiling and flow diversion due to the very wide neck of the aneurysm, arterial tortuosity, and the distortion of the intra-aneurysm thrombus by any endovascular treatment was not recommended. We also expected that the mass effect remains significant after endosaccular coiling.

Even when similar rates of success have been reported, there is controversy about the best site of PAO.[ 13 ] Previous data suggested that occlusion of ICA maximally reduced the pressure and pulsation of the aneurysm minimizing the risk of persistent aneurysm refilling, and the rate of thromboembolism can be lower by decreasing the dead space between the occlusion site and the aneurysm.[ 14 ] Nevertheless, we decided to occlude CCA because ischemic complications have been associated more often with ICA ligation.[ 7 , 14 , 18 , 33 ] The described “safety” of CCA ligation is based on continued patency of the ICA either by anterograde filiform flow or retrograde ECA flow, which may minimize thromboembolic complications from clot formation in the ICA and maintain higher distal perfusion pressure during the perioperative period until collateral flow has been established.

Although ischemic and thromboembolic complications after PAO have received the attention, delayed refilling of ICCA aneurysm could happen. Conventionally, collateral pathway development is based on the proliferation of vasa vasorum induced by neoangiogenic factors after progressive atherothrombotic ICA occlusion.[ 5 , 11 , 19 ] However, Numagami[ 30 ] and Meguro[ 25 ] described how an abrupt occlusion of ICA with coils might be also recanalized through vasa vasorum. One of the first descriptions of the opening of unusual collateral pathways was done by Pelz.[ 10 ] He described in two patients with atherothrombotic occlusion of ICA how the ascending pharyngeal artery functioned as the collateral pathway that maintained the patency of proximally occluded ICAs. It was possible by the anatomic variation of the origin of the ascending pharyngeal artery from the ICA and the anastomoses of its muscular branches with branches originating from the occipital and vertebral arteries.

According to the previous data, two main types of recanalization after PAO may occur:

Retrograde recanalization: backflow of the ophthalmic artery,[ 8 , 37 ] persistent trigeminal artery,[ 6 ] posterior communicating artery, and bypass arteries.[ 4 ] Since the risk of aneurysm rupture is believed to be lower after retrograde recanalization and there was no evidence of aneurysm filling by anterior or posterior communicating arteries in the first angiogram, we did not consider to trap the aneurysm by distal occlusion.

In our opinion, some of the mechanisms that explain the lower risk of thromboembolism and ischemia after CCA occlusion are the same that influence the opening of unusual collaterals. The importance of the evaluation of proximal intracranial ICA branches during the planification of the site of PAO was described by Allen.[ 2 ] He focused on the potential anastomosis between the ECA and branches of the petrous, cavernous, and lacerum portions of the ICA. These proximal branches can explain false negative BTO as the temporal occlusion is usually done at C1-2 level and sources for persistent filling and growth of ICA aneurysms. They recommend performing a second more proximal BTO before deciding where to interrupt the patent artery.

Even with the mentioned multiple sources recanalization of ICCA aneurysms after PAO is a rare complication. If we review the literature of previously reported cases, we identify only seven studies [ Table 1 ]. Opposite to our case, in the vast majority, the collateral pathway was established after revascularization surgery with delayed proximal cervical ICA occlusion.[ 1 , 17 , 27 ] We speculate that flow reduction in the right CCA after PAO led to potential anastomosis between the occipital artery of the ECA and meningeal branches from the right VA in our patient. However, we cannot confirm this mechanism because we did not perform any assessment of cerebral blood flow after ICA occlusion. An alternative explanation is the effect of a giant aneurysm in the parent artery flow that often is distorted/attenuated by the aneurysm and may have a favorable effect in the development of collateral pathways.[ 24 ]

Table 1:

Review of previous cases reporting recanalization of ICCA aneurysm after PAO.

CONCLUSION

Delayed refilling of ICCA aneurysms based on unusual collateral pathway opening after PAO may occur. Periodic long-term follow-up by neuroimaging is recommended, especially in those cases where potential collateral branches of have not been clearly identified in the preoperative studies.

Declaration of patient consent

The authors certify that they have obtained all appropriate patient consent.

Financial support and sponsorship

Nil.

Conflicts of interest

There are no conflicts of interest.

References

1. Abe H, Takemoto K, Higashi T, Inoue T. Surgical treatment for aneurysms in the cavernous-petrous portion of the internal carotid artery. Acta Neurochir Suppl. 2011. 112: 77-83

2. Allen JW, Alastra AJ, Nelson PK. Proximal intracranial internal carotid artery branches: Prevalence and importance for balloon occlusion test. J Neurosurg. 2005. 102: 45-52

3. Ambekar S, Madhugiri V, Sharma M, Cuellar H, Nanda A. Evolution of management strategies for cavernous carotid aneurysms: A review. World Neurosurg. 2014. 82: 1077-85

4. Barnett DW, Barrow DL, Joseph GJ. Combined extracranial-intracranial bypass and intraoperative balloon occlusion for the treatment of intracavernous and proximal carotid artery aneurysms. Neurosurgery. 1994. 35: 92-7

5. Countee RW, Vijayanathan T. External carotid artery in internal carotid artery occlusion. Angiographic, therapeutic, and prognostic considerations. Stroke. 1979. 10: 450-60

6. Drake CG, Peerless SJ, Ferguson GG. Hunterian proximal arterial occlusion for giant aneurysms of the carotid circulation. J Neurosurg. 1994. 81: 656-65

7. Elhammady MS, Wolfe SQ, Farhat H, Ali Aziz-Sultan M, Heros RC. Carotid artery sacrifice for unclippable and uncoilable aneurysms: Endovascular occlusion vs common carotid artery ligation. Neurosurgery. 2010. 67: 1431-6

8. Ezura M, Takahashi A, Yoshimoto T. Combined intravascular parent artery and ophthalmic artery occlusion for giant aneurysms of the supraclinoid internal carotid artery. Surg Neurol. 1997. 47: 360-3

9. Field M, Jungreis CA, Chengelis N, Kromer H, Kirby L, Yonas H. Symptomatic cavernous sinus aneurysms: Management and outcome after carotid occlusion and selective cerebral revascularization. AJNR Am J Neuroradiol. 2003. 24: 1200-7

10. Fox AJ, Viñuela F, Pelz DM, Peerless SJ, Ferguson GG, Drake CG. Use of detachable balloons for proximal artery occlusion in the treatment of unclippable cerebral aneurysms. J Neurosurg. 1987. 66: 40-6

11. Fox JL. Cerebral arterial revascularization: The value of repeated angiography in selection of patients for operation. Neurosurgery. 1978. 2: 205-9

12. Fujiwara S, Fujii K, Fukui M. De novo aneurysm formation and aneurysm growth following therapeutic carotid occlusion for intracranial internal carotid artery (ICA) aneurysms. Acta Neurochir (Wien). 1993. 120: 20-5

13. Giannotta SL, McGillicuddy JE, Kindt GW. Gradual carotid artery occlusion in the treatment of inaccessible internal carotid artery aneurysms. Neurosurgery. 1979. 5: 417-21

14. Heros RC. Thromboembolic complications after combined internal carotid ligation and extra-to-intracranial bypass. Surg Neurol. 1984. 21: 75-9

15. Higashida RT, Halbach VV, Dowd C, Barnwell SL, Dormandy B, Bell J. Endovascular detachable balloon embolization therapy of cavernous carotid artery aneurysms: Results in 87 cases. J Neurosurg. 1990. 72: 857-63

16. Hongo K, Horiuchi T, Nitta J, Tanaka Y, Tada T, Kobayashi S. Double-insurance bypass for internal carotid artery aneurysm surgery. Neurosurgery. 2003. 52: 597-602

17. Kagawa K, Shimizu H, Matsumoto Y, Watanabe M, Tominaga T. Rapid revascularization after therapeutic parent artery occlusion for a large intracavernous carotid artery aneurysm. Neurol Med Chir (Tokyo). 2007. 47: 559-63

18. Kak VK, Taylor AR, Gordon DS. Proximal carotid ligation for internal carotid aneurysms. A long-term follow-up study. J Neurosurg. 1973. 39: 503-13

19. Kemény V, Droste DW, Nabavi DG, Schulte-Altedorneburg G, Schuierer G, Ringelstein EB. Collateralization of an occluded internal carotid artery via a vas vasorum. Stroke. 1998. 29: 521-3

20. Kupersmith MJ, Hurst R, Berenstein A, Choi IS, Jafar J, Ransohoff J. The benign course of cavernous carotid artery aneurysms. J Neurosurg. 1992. 77: 690-3

21. Kurokawa R, Kuroshima Y, Yoshida K, Kawase T. Spontaneous thrombosis of intracavernous internal carotid artery aneurysm and parent artery occlusion in patients with positive balloon test occlusion two case reports. Neurol Med Chir (Tokyo). 2001. 41: 436-41

22. Linskey ME, Sekhar LN, Hirsch W, Yonas H, Horton JA. Aneurysms of the intracavernous carotid artery: Clinical presentation, radiographic features, and pathogenesis. Neurosurgery. 1990. 26: 71-9

23. Linskey ME, Sekhar LN, Horton JA, Hirsch WL, Yonas H. Aneurysms of the intracavernous carotid artery: A multidisciplinary approach to treatment. J Neurosurg. 1991. 75: 525-34

24. Little JR, Rosenfeld JV, Awad IA. Internal carotid artery occlusion for cavernous segment aneurysm. Neurosurgery. 1989. 25: 398-404

25. Meguro T, Muraoka K, Terada K, Hirotsune N, Nishino S. Recanalisation of the internal carotid artery via the vasa vasorum after coil occlusion. Br J Radiol. 2011. 84: e23-6

26. Molyneux AJ, Kerr RS, Yu LM, Clarke M, Sneade M, Yarnold JA. International subarachnoid aneurysm trial (ISAT) of neurosurgical clipping versus endovascular coiling in 2143 patients with ruptured intracranial aneurysms: A randomised comparison of effects on survival, dependency, seizures, rebleeding, subgroups, and aneurysm occlusion. Lancet. 2005. 366: 809-17

27. Nagatani K, Tsuzuki N, Kageyama H, Shima K. Recanalization of a large supraclinoid carotid aneurysm via elicited vertebral artery-internal carotid artery anastomosis: A case report. Turk Neurosurg. 2015. 25: 154-7

28. Nakase H, Shin Y, Kanemoto Y, Ohnishi H, Morimoto T, Sakaki T. Long-term outcome of unruptured giant cerebral aneurysms. Neurol Med Chir (Tokyo). 2006. 46: 379-84

29. Niiro M, Shimozuru T, Nakamura K, Kadota K, Kuratsu J. Long-term follow-up study of patients with cavernous sinus aneurysm treated by proximal occlusion. Neurol Med Chir (Tokyo). 2000. 40: 88-96

30. Numagami Y, Ezura M, Takahashi A, Yoshimoto T. Antegrade recanalization of completely embolized internal carotid artery after treatment of a giant intracavernous aneurysm: A case report. Surg Neurol. 1999. 52: 611-6

31. Puffer RC, Piano M, Lanzino G, Valvassori L, Kallmes DF, Quilici L. Treatment of cavernous sinus aneurysms with flow diversion: Results in 44 patients. AJNR Am J Neuroradiol. 2014. 35: 948-51

32. Raper DM, Ding D, Peterson EC, Crowley RW, Liu KC, Chalouhi N. Cavernous carotid aneurysms: A new treatment paradigm in the era of flow diversion. Expert Rev Neurother. 2017. 17: 155-63

33. Roski RA, Spetzler RF, Nulsen FE. Late complications of carotid ligation in the treatment of intracranial aneurysms. J Neurosurg. 1981. 54: 583-7

34. Shimizu K, Imamura H, Mineharu Y, Adachi H, Sakai C, Tani S. Endovascular parent-artery occlusion of large or giant unruptured internal carotid artery aneurysms. A long-term single-center experience. J Clin Neurosci. 2017. 37: 73-8

35. Stiebel-Kalish H, Kalish Y, Bar-On RH, Setton A, Niimi Y, Berenstein A. Presentation, natural history, and management of carotid cavernous aneurysms. Neurosurgery. 2005. 57: 850-7

36. Taki W, Nishi S, Yamashita K, Sadatoh A, Nakahara I, Kikuchi H. Selection and combination of various endovascular techniques in the treatment of giant aneurysms. J Neurosurg. 1992. 77: 37-42

37. Tatemichi TK, Chamorro A, Petty GW, Khandji A, Oropeza LA, Duterte DI. Hemodynamic role of ophthalmic artery collateral in internal carotid artery occlusion. Neurology. 1990. 40: 461-4

38. Turfe ZA, Brinjikji W, Murad MH, Lanzino G, Cloft HJ, Kallmes DF. Endovascular coiling versus parent artery occlusion for treatment of cavernous carotid aneurysms: A meta-analysis. J Neurointerv Surg. 2015. 7: 250-5

39. van der Schaaf IC, Brilstra EH, Buskens E, Rinkel GJ. Endovascular treatment of aneurysms in the cavernous sinus: A systematic review on balloon occlusion of the parent vessel and embolization with coils. Stroke. 2002. 33: 313-8

40. van Rooij WJ. Endovascular treatment of cavernous sinus aneurysms. AJNR Am J Neuroradiol. 2012. 33: 323-6

41. Wang J, Zheng C, Hou B, Huang A, Zhang X, Du B. Four collateral circulation pathways were observed after common carotid artery occlusion. BMC Neurol. 2019. 19: 201-

42. Wiebers DO, Whisnant JP, Huston J, Meissner I, Brown RD, Piepgras DG. Unruptured intracranial aneurysms: Natural history, clinical outcome, and risks of surgical and endovascular treatment. Lancet. 2003. 362: 103-10