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Atheromatous pseudo-occlusion of the right internal carotid artery
(Portuguese PDF version)

Silvio Romero Barros Marques1, Maria Claudia S. de Albuquerque2, Esdras Marques Lins3, EmanuelleTenório4

1. PhD. Associate professor, Centro de Ciências à Saúde, Universidade Federal de Pernambuco, Recife, PE, Brazil.
2. Substitute professor, Universidade Federal de Pernambuco, Recife, PE, Brazil.
3. Doctoral student, Centro de Ciências à Saúde, Universidade Federal de Pernambuco, Recife, PE, Brazil.
4. Resident physician, Service of Vascular Surgery, Hospital das Clínicas - Universidade Federal de Pernambuco, Recife, PE, Brazil.

Correspondence:
Silvio Romero Barros Marques
Av. Portugal, 163
CEP 52010-010 - Recife, PE, Brazil
Tel.: +55 81 3231.3526
E-mail: silvior.marques@globo.com

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ABSTRACT

The authors report a case of pseudo-occlusion of the right internal carotid artery in a symptomatic patient with severe atheromatous stenosis, which had been diagnosed at the Service of Vascular Surgery of Hospital das Clínicas (Universidade Federal de Pernambuco, Brazil). Angiography evidenced a string sign (or slim sign), which is the characteristic of pseudo-occlusion. This condition is rarely described in medical literature and presents high morbidity and mortality rates. The authors report the aspects related to its diagnosis as well the results of the surgical treatment, and they present a literature review.

Key-words: internal carotid artery, stenosis, angiography.
Palavras-chave: artéria carótida interna, estenose, arteriografia.

J Vasc Br 2004;3(1):43-6

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Pseudo-occlusions of the internal carotid artery are atheromatous lesions with high-grade stenosis, presenting a peculiar arteriographic aspect known as string sign or slim sign. Clinically, pseudo-occlusions present low incidence and high risk for thrombosis and embolism, and are identified by angiographic images when a small quantity of contrast material is injected into the internal carotid artery (ICA).^1-5

Atherosclerosis is the cause of most carotid stenoses and vascular accidents. In more than 70% of the cases, such lesions in the ICA are surgically accessible due to their usual location (between 10 and 30 mm distant from the carotid bulb).⁶

Indications for elective surgery in cases of carotid stenosis are well established in the results of multicentric North-American (NASCET) and European (ESCT) trials, both based on the degree of carotid stenosis and the symptoms of patients.^7,8

In 1970, Lippman et al. reported five cases of internal carotid stenosis greater than or equal to 95%, in which slim signs were identified. In 1990, Fredericks et al. reported internal carotid stenoses of 95% or more in 60 cases. They observed the presence of slim signs in 47% of these cases. The first attempt at categorizing pseudo-occlusion and segmental occlusion of the internal carotid artery was made by Archie in 1994. He established six different categories for 18 surgeries performed in 17 patients, including diameter and fibrotic reaction of the internal carotid artery, carotid plaque and size of the thrombus. There have been other attempts at identifying segmental occlusion and pseudo-occlusion of carotid arteries. However, categorization and adequate management are not yet well established in medical literature.^1,2,9

Horst et al. proposed a simpler categorization for pseudo-occlusion of the carotid artery, based on their 13-year experience with arteriographic and intraoperative findings in 133 patients who underwent surgical procedure due to pseudo-occlusion or segmental occlusion of the internal carotid artery. Thus, they categorized pseudo-occlusion and segmental occlusion as follows:⁸

Type I - subtotal stenosis, with complete anterograde flow in the internal carotid artery.

Type II - total occlusion in the internal carotid artery and in its bifurcation, with delayed anterograde flow in cervical portion and in carotid siphon through unusual collateral vessels of the internal carotid artery (only eventually identified with angiography).

Type III - no image of the cervical segment of the internal carotid artery, patent petrous portion and carotid siphon due to retrograde flow of internal carotid artery through collateral vessels (ophthalmic artery and persistent embryonic arteries).

Type I is initially defined as pseudo-occlusion of the internal carotid artery.

CASE REPORT

Male, 62-year-old, ex-smoker, with hypertension and a history of coronary angioplasty, was admitted in June 2002. His clinical history also included a cerebrovascular accident (1 year and 4 months before), with left hemiparesis, difficulty to walk, dyslalia, deviation of labial commissure to the left secondary to generalized tonicoclonic seizure. It also lead to dizziness and nausea as well as a temporary bilateral auditory deficit, from which he recovered three days after.

Magnetic resonance confirmed the diagnosis of cerebrovascular accident (CVA) in brainstem and white matter bilaterally. Doppler ultrasound of the carotid artery performed on that occasion evidenced diffuse atheromatous disease of the carotid vessels, with stenosis of 50% in the right internal carotid artery, 25% in the right common carotid artery and 45% in the left internal carotid artery.

The patient progressed with partial recovery under physiotherapeutic treatment for 8 months and use of platelet antiaggregant, anti-hypertensive drugs, anticonvulsant and vasodilator medications. One year after, an audiometry was carried out, identifying a bilateral sensory neural loss, especially in the left side. Ultrasound monitoring of cervical arteries was carried out in the same period and evidenced 95% of stenosis in the right internal carotid artery, 70% in the right common carotid artery and 50% in the right vertebral artery. On the contralateral side, the study evidenced a 50% stenosis in the left common carotid artery and a 50 to 70% reduction in lumen size of left internal carotid artery. The left vertebral artery was occluded.

Cerebral and carotid angiography showed subocclusive stenosis in the right internal carotid artery, with distal occlusion at intracranial level and around 50% stenosis in the proximal third of the left internal carotid artery. The patency of the circle of Willis assured the presence of the contrast in the right carotid siphon. The left vertebral artery was occluded in its origin and the right vertebral artery presented subocclusive stenosis, evidencing low flow in the intracranial vertebral-basilar system. Imaging of the right cerebral hemisphere was obtained through selective catheterization of the left internal carotid artery. The patient underwent endarterectomy of the right internal carotid artery, and the ulcerated and friable plaque was removed. The surgery was performed under general anesthesia without any shunt or patch. There was no evidence of intraoperative or postoperative cerebrovascular accident. A postoperative arteriography showed satisfactory functioning of the right carotid bulb and unclogged right internal carotid artery. The patient was discharged on the 9th postoperative day under platelet-antiplatelet therapy.

The 6-month postoperative follow-up with color Doppler ultrasound evidenced patency of the right internal carotid artery (Figures 1 to 4).

Figure 1 - Categorization of segmental occlusion and pseudo-occlusion in the internal carotid artery, modified from Horst et al.⁸

Figure 2 - Arteriography: pseudo-occlusion of the internal carotid artery.

Figure 3 - Ulcerated plaque in right internal carotid artery.

Figure 4 - Postoperative arteriography.

DISCUSSION

Surgical interventions on chronic occlusions of carotid arteries are not recommended by the literature, since the artery, in such a situation, is generally transformed into a fibrous string with no possibility of endarterectomy. However, if total or partial patency is diagnosed in internal carotid artery with pseudo-occlusion or segmental occlusion, it seems to change the prognosis for symptomatic patients.^8,10

The peculiar sign evidenced by the arteriography, known as string sign or slim sign, was found in our patient; the selective arteriography showed a trickle of flow of the contrast material in the internal carotid artery, and reconstitution of the blood flow in the distal portion of the vessel.

The carotid arteries of our patient were initially evaluated with color Doppler ultrasound, which suggested a progressing disease and a severe atheromatous stenosis. However, the examination was not able to inform about the patency of the distal carotid segment, which was actually identified by the arteriography. Some authors argue that a modified color Doppler ultrasound is able to overcome results of standard Doppler ultrasound in the diagnosis of pseudo-occlusion of the carotid artery. Nevertheless, such a special protocol was not available to us.¹¹

Conventional arteriography is usually not adequate to diagnose the patency of internal carotid artery. A digital selective angiography may evidence a retrograde flow (based on delay evaluation) or an anterograde opacification. The string-like blood flow due to partial collapse of the carotid arteries (caused by an important decrease in luminal pressure) leads to false angiographic or ultrasonographic findings of severe stenoses. In cases of segmental lesion, it is relevant to emphasize the importance of selective angiography.¹⁰

In the case reported here, arteriography showed subocclusive stenosis in the right internal carotid artery along with a severe stenosis in the ipsilateral vertebral artery, evidencing an advanced atherosclerosis with risk of another vascular accident. The patient's auditory deficit, as well as his nausea and vomits, may be explained by the atheromas in his vertebral-basilar system.¹²

Facing with reports in medical literature which show the possibility of new thrombotic and embolic episodes in patients with pseudo-occlusion and segmental occlusion of carotid arteries with a surgical risk similar to that of elective surgery, we decided to perform thromboendarterectomy in our patient. Given that the diameter of the carotid bifurcation was large enough, we performed the surgery without any patch. The patient had a postoperative recovery with no evidences of new deficits.¹³

In our experience, the surgical technique for cases involving pseudo-occlusion is somewhat different from usual procedures for endarterectomy. Several maneuvers for cerebral protection, such as the placement of a shunt and evaluation of residual pressure, cannot be performed due to thrombus organization. After clamping common and external carotid arteries, atheroma removal is started without distal clamping; it is performed only when there is adequate reflux through the internal carotid artery. Only then can we decide whether to use or not use an internal shunt, which is usually unnecessary considering the progressive adaptation of cerebral circulation in the contralateral hemisphere.^14-16

CONCLUSION

Pseudo-occlusion of the internal carotid artery is one of the rare situations in which there is urgent indication for carotid endarterectomy. The case reported here leads to the conclusion that surgical results are satisfactory, with asymptomatic recovery of the patients, similarly to cases of transient ischemic attacks, for which elective surgery is indicated.

REFERENCES

1. Lippman HH, Sundt TH, Holman CB. The poststenotic carotid slim sign: spurious internal carotid hypoplasia. Mayo Clin Proc 1970;45:762-7.

2. Fredericks RK, Thomas TD, Lefkowitz DS, et al. Implications of the angiographic string sign in carotid aterosclerosis. Stroke 1990;21:476-9.

3. Azzarrone M, Berni CM, Nahasma BA, et al. Pseudo-occlusion of internal carotid artery. Ann Ital Chir 1996;67(5):621-6.

4. Mehigan JT, Olcot C. The carotid string sign. Differential diagnosis and management. Am J Surg 1980;140:137-43.

5. Regina G, Testini M, Fulone M, et al. Pseudo-occlusion of internal carotid artery: report of 15 cases and review of the literature. Int Angiol 1997;16:147-50.

6. Ringelstein EB, Berg-Dammer E, Zeumer H. The so-called atheromatous pseudo-occlusion of internal carotid artery. A diagnostic and therapeutical challenge. Neuroradiology 1983;25:147-55.

7. Peiper C, Nowack J, Hopstein S, et al. Prophylactic urgent revascularization of the internal carotid artery in the symptomatic patients. Vasa 2001;30:247-51.

8. Kniemeyer HW, Schlachetzki F, Striffeler H, et al. Pseudo-occlusion of the internal carotid artery. Is surgical treatment indicated? In: Chiesa R, Melisano G. La Chirurgia dei Tronchi Sopra Aortici. 1ª ed. Milano: Europa Scienze Umane Editrice; 1997. p. 303-10.

9. Archie JP Jr. Carotid endarterectomy when the distal internal carotid is small or poorly visualized. J Vasc Surg 1994;19:23-30.

10. Thévenet A. Chirurgie des carotides. Encyclopedie Medico-chirurgicale. Techniques Chirurgicales Vasculaires 2002;43143:1-4.

11. Ascher E, Markevich N, Hingorani A, Kallakuri S. Pseudo-occlusions of the internal carotid artery: a rationale for treatment on the basis of a modified carotid duplex scan protocol. J Vasc Surg 2002;35(2):340-5.

12. Kieffer E. Chirurgie de l'atére vertebrale. Encyclopedie Medico-chirurgicale. Techniques Chirurgicales Vasculaires 2002;43130:1-34.

13. Solanich-Valldaura T, Allegue-Allegue N, Arano-Heredero C, Samso JJ, Escribano-Ferrer JM, Matas-Docampo M. Diagnostic and therapeutic management of pseudo-occlusion of the carotid artery. Rev Neurol 2003;36:201-4.

14. Moryenstern LB, Fox AJ, Sharp BC, et al. The risk and benefits of carotid endarterectomy in patients with near occlusion of the carotid artery. North American Symptomatic Carotid Trial (NASCET). Neurology 1997;48:911-5.

15. Berman SS, Bernhard VM, Elly WK, et al. Critical carotid artery stenosis: diagnosis, timing of surgery and outcome. J Vasc Surg 1994;20:409-18.

16. Sekar LN, Heros RC, Rosenbaum AE, et al. Atheromatous pseudo-occlusion of the internal carotid artery. J Neurosurg 1980;52:782-9.