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Duplex ultrasonography evaluation for internal carotid artery restenosis in patients submitted to carotid bifurcation endarterectomy with partial eversion of the internal carotid artery
(Portuguese PDF version)

Fábio Hüsemann Menezes,¹ George Carchedi Luccas,¹ Irene Akie Matsui¹, Andréa Cristina de Oliveira Quim dos Santos¹, Sandra Aparecida Ferreira Silveira²

1. Hospital Centro Médico Campinas, Campinas, SP, Brazil.
2. Radiologia Clínica de Campinas, Campinas, SP, Brazil.

Correspondence:
Fábio Hüsemann Menezes
Rua Deusdeti Martins Gomes, 122
CEP 13084-723 - Campinas, SP, Brazil
Phone: +55 19 3289.3540
Fax: +55 19 3288.0202
E-mail: fmenezes@mpc.com.br

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ABSTRACT

Objective: The aim of the following study is to assess the percentage of the internal carotid artery restenosis, measured by duplex ultrasonography, in the postoperative period of patients submitted to a technical variation of the internal carotid artery endarterectomy.

Method: Thirty-six internal carotid arteries (34 patients) were submitted to carotid artery endarterectomy and intentionally operated by partial eversion of the internal carotid artery. All patients had a duplex ultrasonography (B-mode and velocity evaluation) on the post-operative follow-up.

Results: We found a mean value of stenosis of 22.9%, measured by duplex ultrasonography, in female patients, and 13.3% in male patients (P = 0.034). Only one female patient presented a stenosis of 50% (2.8%).

Conclusions: The authors conclude that the partial eversion is a simple and fast technique, resulting in a low incidence of internal carotid artery stenosis.

Key-words: carotid endarterectomy, carotid stenoses, internal carotid arteries.

J Vasc Br 2005;4(1):47-54

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The surgical approach of the carotid artery has been performed since long ago. Ambroise Pare performed the first carotid artery ligation in 1552.¹Since then the surgery has been through several evolutionary stages, such as ligature, reconstruction with termino-terminal anastomosis, and graft interposition with preserved cadaver vein or artery. Surgical indications were for correcting traumatic injuries, removing head and neck tumors, and treating carotid aneurysms, probably due to the difficulty in diagnosing the occlusive atherosclerotic lesion.¹ After the description of the carotid angiography by Moniz² in 1927, the interest in the carotid artery obstructive disease increased. However, the technical alternatives in the 1930's and 1940's were focused on the internal carotid artery occlusion and consisted basically in the resection of the diseased arterial segment.¹ In the early 1950's, there were new attempts of revascularization of patients with severe cerebral vascular accident and patients with transitory symptoms where the internal carotid artery was not completely obstructed. In 1951, Carrea et al.,³ in Buenos Aires, performed the reconstruction of the internal carotid artery with termino-terminal anastomosis between the distal internal carotid artery and the proximal external carotid artery, but only published the fact in 1955. In 1954, Eastcott et al.,⁴ in London, performed the resection of the bulb with termino-terminal anastomosis of the internal carotid artery in the common carotid artery. However, the first carotid endarterectomy, strictly speaking, was performed by DeBakey⁵ in 1956, through section of the common carotid artery and eversion of the carotid bifurcation. Since the 1960's, the carotid endarterectomy has become popular among American surgeons.^6-11 The open endarterectomy technique, with primary closure or with the use of patch, was then completely widespread and accepted by the medical community. The eversion technique initially used by DeBakey was abandoned, even by the author himself,¹² when it was brought to use again nearly 20 years later by Etheredge¹³ and Jones.¹⁴ Afterwards, Vanmaele et al.¹⁵ and Kieny et al.¹⁶ modified the technique, so that the sectioned and everted carotid would become the internal. This technique was adopted by several authors,^17,18 including in our environment by the team of Miguel Neto et al.,¹⁹ with the attraction of being technically simpler than the open endarterectomy and offering less incidence of recurrent stenosis.^20-22 Nevertheless, another technical alternative, a variant of open endarterectomy, is reported on surgical technique texts, but not on scientific papers on carotid endarterectomy, being clearly adopted by the French team of Thévenet²³ and the American team of Effeney & Stoney's²⁴. Such technique consists of the opening of the carotid bulb and partial eversion of the internal carotid artery through the bulb incision, which was called partial eversion. After the multi-centered studies published in the 1990's,^25-27 which demonstrated the superiority of endarterectomy over the clinical treatment for preventing the cerebral vascular accident, the carotid surgery has been gaining acceptance among vascular surgeons in Brazil. The aim of the present study is to describe the technique of the endarterectomy with partial eversion, comment on its advantages and disadvantages and assess the result in terms of residual stenosis of the internal carotid artery in patients submitted to surgical treatment.

CASUISTICS AND METHOD

Thirty-four patients submitted to carotid endarterectomy with partial eversion were retrospectively studied from April, 1996 to November, 2003, being 22 patients male and 12 female. Two patients were bilaterally operated, in a total of 36 carotid arteries. Mean age was 69 years old in women and 66 years old in men. Mean follow-up time was 19 months. All patients were submitted to ultrasound control in the postoperative period, varying from 1 to 71 months after the initial procedure. The stenosis level was measured through duplex ultrasonography (B-mode imaging with measurement of artery diameter + pulsed Doppler), being considered for calculation the highest value for restenosis described by the ultrasonography within measured values. For instance: between 10% and 20%, 20% was considered. All patients were operated by the same surgical team at a private hospital, referred by the authors' offices and examined by the same ultrasonographer, who had experience in vascular examinations. There were 13 patients excluded from the study in this period. Five patients did not have a control ultrasound, one patient died in the early postoperative due to acute myocardial infarct, six patients were operated using the open technique and one patient presented a distal occlusion of the internal carotid artery right before the cranial base.

The adopted technique was the loco-regional anesthesia associated to intravenous sedation, longitudinal cervicectomy as described by Moore,²⁸ being careful to dissect the internal carotid artery above the end of the atherosclerotic plaque to be removed. The indication for the use of shunt was made by the parameters consciousness and movement of the contralateral upper limb at the side which is being operated. After the systemic heparin administration of 5,000 IU intravenously, the internal, external, and common carotid artery clamping was made. After 4 minutes testing the level of consciousness and movement of the limb, endarterectomy was performed. The technique used consists of the opening of the carotid bulb until immediately before the portion where the internal carotid artery starts having its normal diameter (Figure 1A). We then proceed to the detachment of the atherosclerotic plaque, being extremely careful to enter the internal elastic lamina, since without this lamina it is not possible to proceed to the correct internal carotid artery eversion. The lamina is sectioned at the common carotid artery. We then proceed to the detachment of the external carotid artery plaque (Figure 1B) and finally, through the plaque traction and simultaneous approach of the distal internal carotid artery, the eversion of the internal carotid artery inside the bulb incision is performed, similar to a sock being turned inside out (Figure 1C), until the complete plaque detachment, which should occur without any effort and in such a way that its aspect is like a flute's mouth-piece (Figure 1D and F). The regularization of possible muscle flaps is made, the reflux of the internal carotid artery is tested and the field is irrigated with a heparinized saline solution. Afterwards, the arteriotomy is closed with a 6-0 Prolene continuous suture (Figure 1E), starting at the superior portion (next to the internal carotid artery). Before the suture is tied, clamps should be released. First, the internal carotid artery is released, and then the external carotid artery, allowing a blood reflux through the arteriotomy from both arteries. Next, the suture is tied and the flow of the common carotid artery is released for the external carotid artery and then to the internal carotid artery. As a parameter of technical adjustment, we used only the quality of the pulse in the internal and external carotid arteries after the procedure. In our cases, we reverted half of the administered heparin dose and started the administration of Dextran 40 at a speed of 42 ml/hour. The incision is closed by layers and we use routine closed-suction drainage.

Figure 1 - The internal carotid artery is part of the carotid bulb in its initial portion. The proposed technique consists of opening only this portion of the artery until the point immediately before the carotid artery reaches its normal diameter (A), so that it avoids the suture stenosis (E). After the removal of the external carotid plaque (B), the plaque in the narrowest segment of the internal carotid artery is removed by eversion of the internal carotid artery through bulb arteriotomy (C). Notice the atheroma plaque removed by the partial eversion technique (F), the plaque end shaped as a flute's mouth-piece. This finding reveals that the normal portion of the endothelium was reached in its distal portion.

The comparison between the percentage result of the stenosis in female and male patients was performed by the mean analysis test of Microstat software (Ecosoft Inc, 1984) considering a significant p value if lower than 5%.

RESULTS

The artery clamping mean time was 18 minutes, including 4 minutes of testing. In the present casuistics, the use of temporary blood derivation in any patient was not indicated. All patients had their first postoperative at the Intensive Care Unit, with no cases of vascular cerebral accident. One patient had to return to the surgical center 2 hours after the surgery, due to an expanding cervical hematoma, being detected a muscular artery injury in the path of the suction drain passage. Feeding was started on the procedure evening, and patients were discharged on the fourth postoperative day. The measurement of the restenosis value in the operated internal carotid arteries was in average 16.5%, being 23% female patients and 13% male patients (P = 0.0342), and mean time of ultrasound reassessment 19 months (Table 1, Figure 2).

Table 1 - Table showing the casuistics for the present study. Patients were separated by gender

Name	Age (years old)	Gender	Surgery date	Side	Ultrasound date	% of stenosis	Follow-up (months)
LVG	77	F	Mar/98	L	Nov/02	30	56
MAN	67	F	May/99	L	Jul/02	20	38
YMB	76	F	Jul/99	L	Dec/99	20	5
BMR	67	F	Feb/00	R	Apr/02	40	26
MLS	73	F	Feb/00	R	Apr/02	20	26
TOL	70	F	Aug/00	L	Apr/02	20	20
CFO	74	F	Aug/00	R	Nov/00	40	2
ZVG	70	F	Nov/00	R	Feb/03	15	27
MGS	58	F	May/01	R	Sep/02	0	16
LBC	68	F	Oct/01	L	Mar/02	50	4
MLP	63	F	Nov/01	L	Oct/02	15	11
MFTS	64	F	Nov/01	L	Dec/02	5	13
Mean	69					22.9	20
SR	62	M	Jan/01	R	Jul/03	20	30
PPL	71	M	Apr/96	R	Mar/02	15	71
JFM	63	M	Dec/96	R	Dec/01	0	60
EAF	53	M	Dec/96	R	Nov/97	0	10
OI	65	M	Sep/97	R	Feb/03	0	65
OI	66	M	Feb/98	L	Feb/03	0	60
WK	62	M	May/98	R	Mar/99	30	10
JAM	66	M	Apr/99	L	Sep/00	40	17
ASD	71	M	Jun/99	R	Mar/00	30	8
JA	57	M	Feb/00	R	May/01	40	15
MM	77	M	Sep/00	R	Oct/00	0	1
JSR	54	M	Sep/00	R	Sep/02	10	24
IT	64	M	Feb/01	R	Apr/02	0	14
JPD	62	M	Apr/01	L	Oct/01	30	5
OB	68	M	Jul/01	L	Oct/02	15	15
PVM	51	M	Sep/01	R	Mar/02	30	5
GLS	64	M	Mar/02	R	Aug/02	0	4
OP	75	M	Jul/03	L	Oct/03	20	3
JP	82	M	Jul/03	L	Oct/03	20	3
NBZ	57	M	Nov/03	R	Mar/04	0	3
NBZ	57	M	Jul/03	L	Mar/04	0	7
EM	75	M	May/00	R	Oct/00	0	5
LO	77	M	May/03	R	Aug/03	20	3
JVV	84	M	Jun/03	L	Mar/04	0	9
Mean	66					13.3	25
General Mean	67					16.5	19

 

Figure 2 - Ultrasound result of the stemosis measurement of the internal carotid ateries in operated patients according to categories 0-20%, 21-40%, and above 40%. Male patients are represented in black, female patients are represented in white. Notice that from the ultrasound point of view, only the results above 40% are characterized as stenosis.

DISCUSSION

The carotid endarterectomy is still one of the vascular surgeries most performed in the United States. Besides the classical disputes concerning the type of anesthesia, how to monitor in case shunt is used, and whether the patch should be used for closing endarterectomy, over the past years the literature has presented the debate on open endarterectomy with patch versus endarterectomy with eversion to prevent recurrent stenosis of the carotid artery.^20-22 Nothing has been reported on the partial eversion technique.

This technique, according to our experiment, allows the simplification of the endarterectomy with eversion without losing its qualities in terms of avoiding stenosis of the internal carotid artery by arterial suture. The closure of the bulb arteriotomy is fast and technically simpler than the reanastomosis of the internal carotid artery in the bulb or the confection of an arterial patch. On the other hand, the eversion of the external and internal carotid artery by the opening of the longitudinal arteriotomy of the bulb is technically easier to be performed and achieves the same outcome of the eversion with internal carotid artery section. This technique offers an easier endarterectomy of the external carotid artery through bulb incision. The crucial point for the surgery consists of obtaining the correct lamina of the endarterectomy, which should be the internal elastic lamina, so that it allows a perfect plaque detachment without leaving a distal prominence of the intima-musculature complex that demands fixation points (Figure 3), since it is not possible to apply them with the closed and everted internal carotid artery. After some cases, the form by which the plaque is removed and the visual observation of the plaque, shaped as a flute's mouth-piece (Figure 1F), give the surgeon assurance that the correct lamina has been reached.

Figure 3 - Correct lamina for endarterectomy. The internal elastic plaque should be detached (B), maintaining the muscle layer, so that the distal step of the musculature is avoided, as occurs with the external elastic lamina plane of dissection (A). The intima thickening of the internal carotid artery and the normal external carotid artery can be seen in a transverse cut.

It is important to remember that this technique is easily transformed into the open technique. In case there is the need to place a shunt or fixation points of the distal intima, the extension of the longitudinal arteriotomy of the bulb should be performed, with primary closure or patch, according to the case.

When the recurrent stenosis of the carotid artery is studied, it is important to take into consideration the time between the surgery and the study, the method, and whether the examination was performed only in symptomatic patients or as a routine follow-up.²⁹ Although the recurrent stenosis can be studied by arteriography, duplex ultrasonography is the current choice method for routine follow-up in operated patients. In our casuistics, the anatomical result of the endarterectomy obtained by the semi-eversion technique was excellent, when analyzed by duplex ultrasonography. Observing the internal carotid artery images in B-mode, it is possible to detect small failures on the wall, but they do not compromise the lumen in the vessel. It is interesting to notice that the ultrasonography overestimates the level of stenosis, in such a way that, when the recurrent stenosis is studied by this method, according to Healy & Zierler,³⁰ results with up to 40% of stenosis represent carotid arteries practically normal from the anatomical point of view. Generally speaking, in the studies that deal with this issue, recurrent stenoses are considered the stenoses that compromise more than 50% of the diameter, being considered for surgery only severe stenosis, or above 70%. It is known that in the first 6 months after endarterectomy there is a remodeling of the area submitted to endarterectomy, in a way that around the sixth month there is the highest incidence of abnormal examinations, as a consequence of intimal hyperplasia. Up to 1 year after the surgery there is a reduction in the level of stenosis. It is believed that the stenoses found after the second year are secondary to the progression of the atherosclerotic disease. The failures found immediately after the surgery are a consequence of the lack of complete removal of the atherosclerotic plaque, of intimal flaps and small debris of the residual musculature and secondary to arteriorrhaphy.^31-33 In our casuistics it can be observed that the level of mean residual stenosis was 19% in a mean time of 20 months of follow-up, with images practically normal in B-mode, as can be seen in Figure 4. Only one case in a female patient presented stenosis of 50% at the end of the area submitted to endarterectomy, which can correspond to the incomplete plaque removal. If we took into consideration the incidence of stenoses only equal or above 50%, the incidence of residual stenosis in this casuistics was 2.8%, which is in agreement with the literature.

Figure 4 - Ultrasound image typical of the carotid bifurcation after the surgery by the partial eversion technique, showing the practically normal aspect of the bulb and the most distal internal carotid artery, although the stenosis measurement represents 28%.

Although some authors recommend performing the intraoperative control of the technical quality of the endarterectomy, which can be made by ultrasonography,³⁴ angioscopy³⁵ or arteriography³⁶ in the operating theater, we did not perform intraoperative control in our casuistics, since we do not have angioscopy and ultrasonography in the surgical center and it is not part of the routine performing control arteriography of carotid endarterectomy in awake patients. It is interesting to notice that in these studies the incidence of defects in the distal portion of the area submitted to endarterectomy is similar in the techniques of open endarterectomy and endarterectomy with eversion. Zanetti et al.³⁷ in the EVEREST study (a multi-centered study performed to assess the feasibility and durability of endarterectomy with eversion) analyzed the intraoperative arteriography and angioscopy value in order to modify the result of the endarterectomy. They concluded that the angioscopy shows a better image of the residual anatomical defects, but the resolution of such defects did not result in the improvement of the results, in a way that they do not recommend the routine use of the intraoperative control, pointing out that the technical perfection during the procedure is more important when endarterectomy is performed.

The studies that compare the endarterectomy with eversion to open endarterectomy have shown different results about the incidence of recurrent carotid stenosis. Some of them report a higher incidence in the endarterectomy with eversion, while others report very similar results.^20-22 In these cases, the technical simplicity of the endarterectomy with eversion receives more emphasis than the late result, if compared to the use of patches. We believe that, from the point of view of technical simplicity, the endarterectomy with partial eversion of the internal carotid artery has some advantages, since it associates a simple and small longitudinal arteriotomy, technical facility for plaque removal, a fast procedure and an excellent anatomical result. The great criticism on the partial eversion is the difficulty in directly visualizing the end of the area submitted to endarterectomy, in such a way that, if there are any doubts, the internal carotid artery must be longitudinally opened until the beginning of the normal endothelium. However, as mentioned before, after some practice, the need to widen arteriotomy occurs with very little frequency, being only 13% of operated cases in this period, according to our casuistics.

The same experience has been performed at the Hospital das Clínicas da Universidade Estadual de Campinas over the last 3 years. These cases were excluded from our study due to the diversity of surgeons involved in the surgical act and because the ultrasound controls were not performed by the same researcher. They should be published in the future.

CONCLUSION

The authors conclude that the carotid endarterectomy with partial eversion of the internal carotid artery is one more alternative for performing the carotid bifurcation open surgery, corresponding to a simplification of the technique and associating the advantages of the open endarterectomy techniques to the total eversion of the internal carotid artery through its complete sectioning.

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