Recurrence of an extracranial internal carotid artery aneurysm treated with STA-MCA bypass and trapping due to neovascularization from an ascending pharyngeal artery: illustrative case

Keijiro Shomura Department of Neurosurgery, Fukui Prefectural Hospital, Fukui, Japan
Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan

Search for other papers by Keijiro Shomura in
Current site
jns
Google Scholar
PubMed
Close
 MD
,
Tomoya Kamide Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan

Search for other papers by Tomoya Kamide in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Takehiro Uno Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan
Department of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Japan

Search for other papers by Takehiro Uno in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Kouichi Misaki Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan

Search for other papers by Kouichi Misaki in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Satoko Nakada Department of Diagnostic Pathology, Kanazawa University Hospital, Kanazawa, Japan
Department of Pathology and Laboratory Medicine, Hokuriku Brain and Neuromuscular Disease Center, National Hospital Organization Iou National Hospital, Kanazawa, Japan

Search for other papers by Satoko Nakada in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Yukinobu Ito Department of Diagnostic Pathology, Kanazawa University Hospital, Kanazawa, Japan

Search for other papers by Yukinobu Ito in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Hemragul Sabit Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan

Search for other papers by Hemragul Sabit in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Akifumi Yoshikawa Department of Neurosurgery, Kanazawa Medical University, Uchinada, Ishikawa, Japan; and

Search for other papers by Akifumi Yoshikawa in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Masanao Mohri Department of Neurosurgery, Toyama City Hospital, Toyama, Japan

Search for other papers by Masanao Mohri in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
,
Naoyuki Uchiyama Department of Neurosurgery, Ishikawa Prefectural Central Hospital, Kanazawa, Japan

Search for other papers by Naoyuki Uchiyama in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
, and
Mitsutoshi Nakada Department of Neurosurgery, Graduate School of Medical Science, Kanazawa University, Kanazawa, Japan

Search for other papers by Mitsutoshi Nakada in
Current site
jns
Google Scholar
PubMed
Close
 MD, PhD
Open access

BACKGROUND

Extracranial internal carotid artery aneurysms (EICAs) are rare. Although a high mortality risk has been reported in nonoperated cases, the optimal treatment for EICAs remains unknown.

OBSERVATIONS

A 79-year-old female presented with painless swelling in the right neck. Imaging revealed a giant EICA with a maximum diameter of 3.2 cm. Superficial temporal artery–middle cerebral artery bypass and internal carotid artery (ICA) trapping were performed. Because the distal aneurysm edge was at the C1 level, the distal portion of the aneurysm was occluded by endovascular coiling, and the proximal portion was surgically ligated. Blood flow into the aneurysm disappeared after the operation. Three years postsurgery, enlargement of the aneurysm with blood flow from the ascending pharyngeal artery (APA) was detected. The EICA was resected after coiling the APA and ligating both ends of the aneurysm. Pathologically, neovascularization within the aneurysm wall was observed.

LESSONS

Even if blood flow into an EICA disappears after ICA trapping, the EICAs can enlarge due to neovascularization from the neighboring artery. From the outset, removal of the aneurysm should be considered as a radical treatment strategy for giant EICAs.

ABBREVIATIONS

APA = ascending pharyngeal artery; CCA = common carotid artery; EICA = extracranial internal carotid artery aneurysm; Gd = gadolinium; ICA = internal carotid artery; MCA = middle cerebral artery; MRI = magnetic resonance imaging; STA = superficial temporal artery

BACKGROUND

Extracranial internal carotid artery aneurysms (EICAs) are rare. Although a high mortality risk has been reported in nonoperated cases, the optimal treatment for EICAs remains unknown.

OBSERVATIONS

A 79-year-old female presented with painless swelling in the right neck. Imaging revealed a giant EICA with a maximum diameter of 3.2 cm. Superficial temporal artery–middle cerebral artery bypass and internal carotid artery (ICA) trapping were performed. Because the distal aneurysm edge was at the C1 level, the distal portion of the aneurysm was occluded by endovascular coiling, and the proximal portion was surgically ligated. Blood flow into the aneurysm disappeared after the operation. Three years postsurgery, enlargement of the aneurysm with blood flow from the ascending pharyngeal artery (APA) was detected. The EICA was resected after coiling the APA and ligating both ends of the aneurysm. Pathologically, neovascularization within the aneurysm wall was observed.

LESSONS

Even if blood flow into an EICA disappears after ICA trapping, the EICAs can enlarge due to neovascularization from the neighboring artery. From the outset, removal of the aneurysm should be considered as a radical treatment strategy for giant EICAs.

ABBREVIATIONS

APA = ascending pharyngeal artery; CCA = common carotid artery; EICA = extracranial internal carotid artery aneurysm; Gd = gadolinium; ICA = internal carotid artery; MCA = middle cerebral artery; MRI = magnetic resonance imaging; STA = superficial temporal artery

Extracranial internal carotid artery aneurysms (EICAs) are rare.1–4 They have multiple causes, including atherosclerosis, fibromuscular dysplasia, trauma, iatrogenic lesions, infections, congenital defects, and neck irradiation.5,6 EICAs can cause severe complications due to rupture, thrombosis, or embolism. However, there is no consensus on the optimal treatment for EICA. Herein, we report the case of an EICA that was trapped by coiling and ligation but subsequently recurred by neovascularization from the ascending pharyngeal artery (APA).

Illustrative Case

Clinical History and Examination

A 79-year-old female presented to our hospital with a painless right-sided cervical mass. She had no history of trauma, infection, tumor, or surgical intervention in the neck. Magnetic resonance imaging (MRI) revealed a giant EICA with a maximum diameter of 3.2 cm (Fig. 1A). Angiography of the right common carotid artery (CCA) revealed blood flow into the aneurysm (Fig. 1B). The distal portion of the aneurysm was at the C1 level (Fig. 1C). Because the aneurysm was large, and the risk of stroke was considered high, the decision was made to eliminate the blood flow into the aneurysm.

FIG. 1
FIG. 1

Coronal T1-weighted imaging (A) shows a giant EICA with a maximum diameter of 3.0 cm on the right side. Right CCA angiogram before the first operation (B) shows blood flow into the aneurysm. Three-dimensional rotational angiogram (C) shows that the distal end of the aneurysm was as high as the C1 level. On the distal side of the aneurysm (D), we performed internal trapping with endovascular coil embolization (white arrows), and the proximal side was ligated with 1–0 silk thread (E). Angiogram obtained after the first surgery showed that the STA-MCA bypass was patent (black arrowheads) and that blood flow into the aneurysm had completely disappeared (F, black arrows). An = aneurysm; ECA = external carotid artery.

First Operation

First, a superficial temporal artery–middle cerebral artery (STA-MCA) bypass was performed to prevent cerebral infarction. Subsequently, trapping was performed. The distal side of the aneurysm seemed too high to expose and ligate. Therefore, we performed trapping using a combination of endovascular and surgical methods. We embolized the distal part with coiling (Fig. 1D) and ligated the proximal portion with a 1–0 silk thread (Fig. 1E). Postoperative angiography confirmed that the STA-MCA bypass was patent, and blood flow into the aneurysm had disappeared. Finally, we punctured the aneurysm with a 23-gauge needle and aspirated 3 mL of blood for decompression. All surgeries were performed on the same day in a hybrid operating room. Postoperatively, the patient was discharged without neurological deficits.

Aneurysm Recurrence

Three years after surgery, the patient noticed that her right cervical mass began to swell. Follow-up MRI revealed enlargement of the aneurysm (Fig. 2A and B). The aneurysm wall was strongly enhanced and thickened on gadolinium (Gd)-enhanced T1-weighted images (Fig. 2C). Right CCA angiography revealed blood flow from a serpiginous artery from the enlarged APA (Fig. 3). Therefore, we decided to resect the aneurysm to prevent further growth.

FIG. 2
FIG. 2

Coronal MRI performed 3 months (A) and 3 years after the initial surgery (B), showing growth of the aneurysm (white arrows) and increased swelling of the right neck (white arrowheads). Gd-enhanced T1-weighted imaging shows a strongly enhanced aneurysm wall (C).

FIG. 3
FIG. 3

Imaging findings at the recurrence. A right CCA angiogram (A), arterial phase, shows a straight artery (black arrowheads) and serpiginous blood vessel (white arrowheads). In contrast, the venous phase shows blood flow into the aneurysm (B). A three-dimensional rotational angiogram shows that the serpiginous artery (white arrowheads) is from the enlarged APA (black arrowheads, C).

Second Operation

We first performed endovascular embolization of the main feeding artery from the APA to reduce intraoperative bleeding. Superselection of the feeding artery with microcatheters was performed, and N-butyl 2-cyanoacrylate and a detachable coil were used to embolize the APA (Fig. 4A–C). The previous skin incision was extended to the mastoid process and added to anteriorly, exposing the aneurysm (Fig. 4D). Additionally, we excised the digastric muscle and confirmed the distal edge of the aneurysm (Fig. 4E). Finally, the proximal and distal internal carotid arteries (ICAs) were ligated with a 1–0 silk thread, and the aneurysm was resected (Fig. 4F). The postoperative course was uneventful, and the patient was discharged without any neurological deficits. The patient has been under follow-up for 4 years, and no recurrence has been observed.

FIG. 4
FIG. 4

Intraoperative findings during the second surgery, including views of endovascular treatments (A–C) and open surgical treatments (D–F). Superselection of the feeding artery with microcatheters was made, and N-butyl 2-cyanoacrylate was injected into the feeder (A). Part of the APA was embolized by coils so as not to immigrate normal arteries via various anastomoses (white arrows, B). Angiogram after the embolization (C) shows slight blood flow in the APA (black arrowheads) and the aneurysm. The aneurysm, ECA, and CCA were exposed (D). The distal side of the aneurysm was ligated with 1–0 silk thread (E), and the aneurysm was resected (F).

Pathological Findings

The aneurysm was 3.3 cm in size, saccular in shape (Fig. 5A), and contained a reddish-brown, partially white thrombus. The wall of the aneurysm was thickened fibrously (Fig. 5B and C). Histologically, the thrombus had fibrin, erythrocytes, and recanalization consisting of capillary and small vessels. There was organization and it was speculated that blood flow had been continued in the area occupied by red blood cells. The intima was thickened by fibrosis with a few capillaries and mild atherosclerotic changes. The medial elastic tissue was fragmented with mucous degeneration and had capillaries and small vessels with elastic fibers. In the marginal area, arterioles with a diameter of 1 mm were seen, and fibroblast-like cells were often seen in the wall (Fig. 5D–F). No inflammation was observed. Immunohistochemically, many new blood vessels in the vessel wall were positive for CD34 (Fig. 5G) and negative for CD31 (Fig. 5H) and D2–40 (Fig. 5I). Double immunofluorescence also showed that the endothelial cells were positive for CD34 and negative for CD31 (Fig. 5J–M).

FIG. 5
FIG. 5

The cut surface of the ICA aneurysm (A). The aneurysm contained a mostly reddish brown, partially white hematoma. The wall of the aneurysm was thickened. Whole sections of the aneurysm (B, C). There were many vessels with red blood cells and neovascularization. The wall of the aneurysm was fibrously thickened and had a few vessels with elastic fibers. High-power views of the aneurysm wall (D–I). In the hematoma, there were many neovascularized vessels. Endothelium of neovascularized vessels were positive for CD34 (G) and negative for CD31 (H) and D2–40 (I). In the media, there were several small vessels with or without elastic fibers (E). There was mucin deposition in the external region of the media (F). Double immunofluorescence of the microvessels in the aneurysm wall (J–M). The microvessels were positive for CD34 (J) and negative for CD31 (K). Hematoxylin and eosin (B and D), Elastica-Masson (C and E), Alcian Blue (pH 2.5, F), DAPI (L), and merged (M). Original magnification ×2 (D–F) and ×40 (G–I). Bar = 5 mm (B and C) and 50 µm (J–M).

Patient Informed Consent

The necessary patient informed consent was obtained in this study.

Discussion

EICAs are a rare disorder. Early reports show a 60% to 70% mortality rate with conservative therapies and a 50% stroke rate in the natural history of EICAs.7,8 Both medical and interventional methods have been reported for treating these aneurysms. Medical therapy includes antithrombotic treatment and regular follow-up. Interventional therapies include open surgery (ligation or resection) and endovascular treatments.3,6 Removal of the EICA is a radical surgery; however, it has a high risk of cranial nerve damage. Endovascular treatments such as coil embolization, stenting, and parent artery occlusion are minimally invasive and are associated with fewer postoperative complications; however, there are very few reports with long-term observation, and the postoperative course is unclear.

In the case reported herein, recanalization into the trapped aneurysm occurred by a feeding artery from the APA, and many small arteries were seen in the aneurysm wall. Pathological examination was performed to determine how those arteries were formed. We performed double immunofluorescence of the small arteries seen in the aneurysm wall and found that they were positive for CD34 but negative for CD31. Both CD34 and CD31 are markers of blood endothelial cells. In addition, it is known that CD34 is a marker of immature endothelial cells, and CD31 is a marker of mature endothelial cells.9 This suggests that the small arteries in the aneurysm wall were immature; that is, they were not developed from originally existing vessels, but were newly created.

We believe that increased blood demand of the trapped aneurysm wall induced the angiogenesis in this case. The question is how the trapped aneurysm wall had survived until the angiogenesis occurred. We considered that vasa vasorum played an important role.

Vasa vasorum are a network of microvessels located in the vessel walls of mid- to large-sized arteries.10–13 The vasa vasorum supply oxygen and nutrients to the adventitia and the outer media of the arterial wall. In contrast, the intima and inner media are nourished directly from the arterial lumen.13 Previous research has shown that healthy intracranial arteries mostly lack vasa vasorum (except for the central side of the ICA and vertebral artery), and they are relatively rich in cervical arteries.10,14 This difference is clinically important. During the first surgery in our case, ligation was performed for the proximal side of the aneurysm, and the blood flow from the proximal side was completely blocked. On the other hand, coil embolization was performed for the distal side, and blood flow from the artery lumen was blocked; however, blood flow from the vessel wall (from the vasa vasorum) remained. The mechanism of the recurrence may be as follows: after the first surgery, vasa vasorum from the distal ICA nourished the aneurysm wall. Then, neovascularization occurred from the APA into the aneurysm wall to supplement blood flow. New vessels from the APA gradually developed and formed a serpiginous appearance and, finally, recanalized the aneurysm. In one report using a rabbit model, when the arterial wall of a carotid artery was patched to a jugular vein and exposed to a relatively hypoxic environment, the attached arterial wall induced angiogenesis from the nearby artery.15 The arterial wall of carotid arteries may have the potential to induce angiogenesis from nearby arteries when they are exposed to ischemia or hypoxia.

Observations

We present the case of an EICA that was trapped by coiling at the distal side and ligation at the proximal side but still enlarged due to the feeding artery from the APA. Pathological findings suggested that the arteries within the aneurysm were immature, and that angiogenesis had occurred. This is the first report describing a trapped EICA causing a recurrence by inducing feeders from a nearby artery.

Lessons

This report suggests that resection may be preferable for the radical treatment of EICA. In particular, considering that vasa vasorum exist in extracranial carotid arteries, endovascular treatments alone could be insufficient for EICA.

Author Contributions

Conception and design: Kamide, Shomura. Acquisition of data: Kamide, Shomura, Uno, Nakada, Ito, Sabit, Mohri. Analysis and interpretation of data: Shomura, Nakada, Ito, Uchiyama. Drafting the article: Shomura, Nakada. Critically revising the article: Kamide, Shomura, Misaki, Nakada, Ito, Nakada. Reviewed submitted version of manuscript: Kamide, Shomura, Uno, Misaki, Yoshikawa, Nakada. Approved the final version of the manuscript on behalf of all authors: Kamide. Administrative/technical/material support: Sabit. Study supervision: Shomura, Ito, Uchiyama.

References

  • 1

    Alpagut U, Ugurlucan M, Kafali E, et al. Aneurysm of the kinked extracranial internal carotid artery case report and review of the literature. Acta Chir Belg. 2005;105(4):407409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Houser OW, Baker HL Jr. Fibromuscular dysplasia and other uncommon diseases of the cervical carotid artery: angiographic aspects. Am J Roentgenol Radium Ther Nucl Med. 1968;104(1):201212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Welleweerd JC, den Ruijter HM, Nelissen BGL, et al. Management of extracranial carotid artery aneurysm. Eur J Vasc Endovasc Surg. 2015;50(2):141147.

  • 4

    McCollum CH, Wheeler WG, Noon GP, DeBakey ME Aneurysms of the extracranial carotid artery. Twenty-one years’ experience. Am J Surg. 1979;137(2):196200.

  • 5

    Reslan OM, Ebaugh JL, Raffetto JD Bilateral asymptomatic extracranial carotid artery aneurysms. Ann Vasc Surg. 2010;24(5):691.e11–6.

  • 6

    Fankhauser GT, Stone WM, Fowl RJ, et al. Surgical and medical management of extracranial carotid artery aneurysms. J Vasc Surg. 2015;61(2):389393.

  • 7

    de Jong KP, Zondervan PE, van Urk H Extracranial carotid artery aneurysms. Eur J Vasc Surg. 1989;3(6):557562.

  • 8

    Yoneyama T, Kawashima A, Sugiura M, et al. Technical options for the surgical management of extracranial carotid artery aneurysms. Three case reports. Neurol Med Chir (Tokyo). 2012;52(4):208212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Nagatsuka H, Hibi K, Gunduz M, et al. Various immunostaining patterns of CD31, CD34 and endoglin and their relationship with lymph node metastasis in oral squamous cell carcinomas. J Oral Pathol Med. 2005;34(2):7076.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Wen D, Kieran NW, Yu Z, et al. Presence of vasa vasorum in human intracranial aneurysms. Acta Neurochir (Wien). 2020;162(9):22832293.

  • 11

    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(998):e23e26.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Iampreechakul P, Wangtanaphat K, Lertbutsayanukul P, Siriwimonmas S Revascularization of the internal carotid artery through the hypertrophied vasa vasorum in traumatic carotid-cavernous fistula previously treated by ligation of cervical carotid arteries: A case report. Surg Neurol Int. 2022;13:324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Sedding SG, Boyle EC, Demandt JAF, et al. Vasa vasorum angiogenesis: key player in the initiation and progression of atherosclerosis and potential target for the treatment of cardiovascular disease. Front Immunol. 2018;9:706.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Aydin F Do human intracranial arteries lack vasa vasorum? A comparative immunohistochemical study of intracranial and systemic arteries. Acta Neuropathol. 1998;96(1):2228.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Ito Y, Yoshida M, Maeda D, et al. Neovasculature can be induced by patching an arterial graft into a vein: a novel in vivo model of spontaneous arteriovenous fistula formation. Sci Rep. 2018;8(1):3156.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • Collapse
  • Expand
  • FIG. 1

    Coronal T1-weighted imaging (A) shows a giant EICA with a maximum diameter of 3.0 cm on the right side. Right CCA angiogram before the first operation (B) shows blood flow into the aneurysm. Three-dimensional rotational angiogram (C) shows that the distal end of the aneurysm was as high as the C1 level. On the distal side of the aneurysm (D), we performed internal trapping with endovascular coil embolization (white arrows), and the proximal side was ligated with 1–0 silk thread (E). Angiogram obtained after the first surgery showed that the STA-MCA bypass was patent (black arrowheads) and that blood flow into the aneurysm had completely disappeared (F, black arrows). An = aneurysm; ECA = external carotid artery.

  • FIG. 2

    Coronal MRI performed 3 months (A) and 3 years after the initial surgery (B), showing growth of the aneurysm (white arrows) and increased swelling of the right neck (white arrowheads). Gd-enhanced T1-weighted imaging shows a strongly enhanced aneurysm wall (C).

  • FIG. 3

    Imaging findings at the recurrence. A right CCA angiogram (A), arterial phase, shows a straight artery (black arrowheads) and serpiginous blood vessel (white arrowheads). In contrast, the venous phase shows blood flow into the aneurysm (B). A three-dimensional rotational angiogram shows that the serpiginous artery (white arrowheads) is from the enlarged APA (black arrowheads, C).

  • FIG. 4

    Intraoperative findings during the second surgery, including views of endovascular treatments (A–C) and open surgical treatments (D–F). Superselection of the feeding artery with microcatheters was made, and N-butyl 2-cyanoacrylate was injected into the feeder (A). Part of the APA was embolized by coils so as not to immigrate normal arteries via various anastomoses (white arrows, B). Angiogram after the embolization (C) shows slight blood flow in the APA (black arrowheads) and the aneurysm. The aneurysm, ECA, and CCA were exposed (D). The distal side of the aneurysm was ligated with 1–0 silk thread (E), and the aneurysm was resected (F).

  • FIG. 5

    The cut surface of the ICA aneurysm (A). The aneurysm contained a mostly reddish brown, partially white hematoma. The wall of the aneurysm was thickened. Whole sections of the aneurysm (B, C). There were many vessels with red blood cells and neovascularization. The wall of the aneurysm was fibrously thickened and had a few vessels with elastic fibers. High-power views of the aneurysm wall (D–I). In the hematoma, there were many neovascularized vessels. Endothelium of neovascularized vessels were positive for CD34 (G) and negative for CD31 (H) and D2–40 (I). In the media, there were several small vessels with or without elastic fibers (E). There was mucin deposition in the external region of the media (F). Double immunofluorescence of the microvessels in the aneurysm wall (J–M). The microvessels were positive for CD34 (J) and negative for CD31 (K). Hematoxylin and eosin (B and D), Elastica-Masson (C and E), Alcian Blue (pH 2.5, F), DAPI (L), and merged (M). Original magnification ×2 (D–F) and ×40 (G–I). Bar = 5 mm (B and C) and 50 µm (J–M).

  • 1

    Alpagut U, Ugurlucan M, Kafali E, et al. Aneurysm of the kinked extracranial internal carotid artery case report and review of the literature. Acta Chir Belg. 2005;105(4):407409.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 2

    Houser OW, Baker HL Jr. Fibromuscular dysplasia and other uncommon diseases of the cervical carotid artery: angiographic aspects. Am J Roentgenol Radium Ther Nucl Med. 1968;104(1):201212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 3

    Welleweerd JC, den Ruijter HM, Nelissen BGL, et al. Management of extracranial carotid artery aneurysm. Eur J Vasc Endovasc Surg. 2015;50(2):141147.

  • 4

    McCollum CH, Wheeler WG, Noon GP, DeBakey ME Aneurysms of the extracranial carotid artery. Twenty-one years’ experience. Am J Surg. 1979;137(2):196200.

  • 5

    Reslan OM, Ebaugh JL, Raffetto JD Bilateral asymptomatic extracranial carotid artery aneurysms. Ann Vasc Surg. 2010;24(5):691.e11–6.

  • 6

    Fankhauser GT, Stone WM, Fowl RJ, et al. Surgical and medical management of extracranial carotid artery aneurysms. J Vasc Surg. 2015;61(2):389393.

  • 7

    de Jong KP, Zondervan PE, van Urk H Extracranial carotid artery aneurysms. Eur J Vasc Surg. 1989;3(6):557562.

  • 8

    Yoneyama T, Kawashima A, Sugiura M, et al. Technical options for the surgical management of extracranial carotid artery aneurysms. Three case reports. Neurol Med Chir (Tokyo). 2012;52(4):208212.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 9

    Nagatsuka H, Hibi K, Gunduz M, et al. Various immunostaining patterns of CD31, CD34 and endoglin and their relationship with lymph node metastasis in oral squamous cell carcinomas. J Oral Pathol Med. 2005;34(2):7076.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 10

    Wen D, Kieran NW, Yu Z, et al. Presence of vasa vasorum in human intracranial aneurysms. Acta Neurochir (Wien). 2020;162(9):22832293.

  • 11

    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(998):e23e26.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 12

    Iampreechakul P, Wangtanaphat K, Lertbutsayanukul P, Siriwimonmas S Revascularization of the internal carotid artery through the hypertrophied vasa vasorum in traumatic carotid-cavernous fistula previously treated by ligation of cervical carotid arteries: A case report. Surg Neurol Int. 2022;13:324.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 13

    Sedding SG, Boyle EC, Demandt JAF, et al. Vasa vasorum angiogenesis: key player in the initiation and progression of atherosclerosis and potential target for the treatment of cardiovascular disease. Front Immunol. 2018;9:706.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 14

    Aydin F Do human intracranial arteries lack vasa vasorum? A comparative immunohistochemical study of intracranial and systemic arteries. Acta Neuropathol. 1998;96(1):2228.

    • PubMed
    • Search Google Scholar
    • Export Citation
  • 15

    Ito Y, Yoshida M, Maeda D, et al. Neovasculature can be induced by patching an arterial graft into a vein: a novel in vivo model of spontaneous arteriovenous fistula formation. Sci Rep. 2018;8(1):3156.

    • PubMed
    • Search Google Scholar
    • Export Citation

Metrics

All Time Past Year Past 30 Days
Abstract Views 0 0 0
Full Text Views 297 297 50
PDF Downloads 237 237 24
EPUB Downloads 0 0 0