Abstract
Objective
In the present study, we summarize our experience in locating the nidus of arteriovenous malformations (AVMs) with a dominant outflow vein (DOV) in the lower extremities and eradicating the nidus with ethanol and coils.
Methods
Twelve patients with lower extremity AVMs who underwent ethanol embolization combined with DOV occlusion from January 2017 to May 2018 were enrolled in the present study. Selective angiography was used to locate the nidus of the AVMs, which was eradicated using ethanol and coils via the direct puncture pathway. All treated patients underwent postoperative follow-up (mean, 25.5 months; range, 14-37 months).
Results
The 12 patients underwent a total of 29 procedures (mean, 2.4; range, 1-4) with 27 detachable coils and 169 Nester coils (Cook Medical Inc, Bloomington, IN). Of the 12 patients, 7 (58.3%) had a complete response and 5 (41.7%) a partial response. Three patients (25%) had minor complications such as blister and superficial skin ulcers during follow-up. However, they recovered spontaneously and completely. No major complications were recorded.
Conclusions
Ethanol embolization combined with coil-assisted DOV occlusion has the potential to eradicate the nidus of lower extremity AVMs with acceptable complication rates.
Keywords: Accessory, Microfoam, Radiofrequency ablation, Saphenous, Varicose vein, Venous ulcer
Article Highlights.
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Type of Research: A single-center, retrospective cohort study
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Key Findings: Twelve patients with arteriovenous malformations in the lower extremities underwent 29 ethanol embolization procedures (mean, 2.4; range, 1-4) with 27 detachable coils and 169 Nester coils. Of the 12 patients, 7 (58.3%) exhibited a complete response and 5 (41.7%) a partial response.
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Take Home Message: Ethanol embolization combined with coil-assisted dominant outflow vein occlusion has the potential to eradicate the nidus of arteriovenous malformations in the lower extremities with an acceptable risk of complications.
Arteriovenous malformations (AVMs) are high-flow vascular anomalies characterized by hypertrophied inflow arteries shunting into dilated and, usually multiple, outflow veins through a primitive vascular nidus. The treatment of AVMs depends on a thorough assessment of the clinical signs and shunt type and a detailed understanding of the angioarchitecture. Imaging studies have allowed us to better understand the angioarchitecture of the nidus to optimize therapies and minimize the risks of endovascular treatment. Embolization has emerged as the primary mode of therapy for AVMs with improvements in catheter delivery systems and embolic agents.1,2
The primary goal of treatment for AVMs is to maximize the control of shunting and to alleviate clinical manifestations. However, every effort must be made to eradicate the “nidus” of the arteriovenous communication, rather than occluding the feeding vessels.3, 4, 5 The concept of “nidus,” a Latin term meaning “nest,” was first proposed by Doppman3 in 1971 when reporting an angiographic review of a series of spinal cord AVMs. Doppman3 described the nidus as “the point toward which multiple feeding arteries converge and from which enlarged veins drain. It is, in essence, the fundamental lesion, or the basic vascular pathology.” This definition remains the most accurate description of a “nidus.” An abnormal region of the arterial and venous vessel connection that creates low perfusion pressure is clinically referred to as the nidus. As described by Doppman,3 three angiographic signs can be used to locate the nidus: (1) junction of multiple arterial feeders; (2) a divergent point of bidirectional venous drainage; and (3) the site of an abrupt increase in the blood vessel diameter.
Among the various types of AVMs, whether using the Cho or Yakes classification, AVMs with a dominant outflow vein (DOV) are more difficult to treat using a liquid embolic agent alone, because the injected agent, such as ethanol, can be rapidly excreted through the DOV.6,7 However, this type also has the highest possibility of cure because coiling can be combined with ethanol, in contrast to other types.
In the present study, we retrospectively assessed the therapeutic outcomes of the identification and eradication of the AVM nidus using coils and absolute ethanol in the lower extremities of patients with a DOV.
Methods
Patients
The present study was conducted at our multidisciplinary tertiary referral Center for Vascular Anomalies in Shanghai Ninth People's Hospital. The committee on clinical investigation of our hospital reviewed and approved the present study. The included patients provided written informed consent for the use of their photographs and clinical information. Twelve consecutive patients with lower extremity AVMs who had undergone ethanol embolization with coil-assisted DOV occlusion between January 2017 and May 2018 were enrolled. The exclusion criteria were as follows: (1) previous embolization or feeding artery ligation; and (2) extensive anatomic structures that affected the soft tissue and bone. For participants who were minors (age <16 years), their parents provided written informed consent.
Angiographically, AVMs with a DOV are defined as multiple arteriolar of the nidus shunting into dilated veins. We enrolled 12 patients (4 males and 8 females), with a mean age of 31.7 years (range, 13-48 years) in the present study (Table I). All patients exhibited a variety of symptoms. The most common symptoms were swelling, pulsation and/or thrill, and dysfunction of the lower extremities (Table I).
Table I.
Baseline patient characteristics
| Pt. no. | Age, years/sex | Schobinger stage | Location | Clinical manifestations |
|---|---|---|---|---|
| 1 | 37/Male | II | Thigh | Swelling, pulsation or thrill |
| 2 | 48/Male | II | Lower leg | Swelling, dysfunction |
| 3 | 33/Female | III | Foot | Swelling, pulsation or thrill |
| 4 | 13/Female | III | Foot | Swelling, pulsation or thrill |
| 5 | 28/Female | II | Lower leg | Swelling, pulsation or thrill, dysfunction |
| 6 | 23/Male | II | Thigh | Swelling, warmth |
| 7 | 36/Female | II | Lower leg | Swelling, pulsation or thrill |
| 8 | 44/Male | II | Thigh | Swelling, pulsation or thrill |
| 9 | 27/Female | III | Lower leg | Swelling, pulsation or thrill, dysfunction |
| 10 | 32/Female | III | Foot | Swelling, pulsation or thrill |
| 11 | 23/Female | II | Foot | Swelling, dysfunction |
| 12 | 36/Female | II | Lower leg | Swelling, pulsation or thrill |
Pt. No., Patient number.
We used the Schobinger staging criteria adopted by the International Society for the Study of Vascular Anomalies for the clinical evaluation of AVMs. Of the 12 patients, 8 had Schobinger stage II AVMs (75%) and 4 had Schobinger stage III AVMs (25%; Table I). After the initial clinical examination, contrast-enhanced computed tomography was recommended to evaluate the hemodynamic and anatomic features (Fig 1). Before embolization, superselective digital subtraction angiography (DSA) was used to identify the feeding arteries, nidus, and drainage veins. The patients’ gender, age, Schobinger stage, lesion site, and clinical manifestations were recorded (Table I).
Fig 1.
Contrast-enhanced computed tomography image showing enhancement of the nidus of the arteriovenous malformation (AVM) centered in the left lower leg (arrow).
Endovascular techniques
All embolization procedures were performed with the patient under general anesthesia via nasal intubation. Oxygen saturation, invasive arterial pressure, and end-tidal carbon dioxide levels and the electrocardiogram were constantly monitored throughout the procedure.
Locating the AVM nidus and DOV
All patients underwent angiography of the related artery (primarily the femoral and posterior tibial arteries) via a femoral approach to determine the detailed angioarchitecture of the AVM. The angiographic images were carefully observed frame by frame and divided into three phases: arterial, nidus, and venous. The arterial phase was defined as the primary manifestation of the supplying arteries (single or multiple) with a branch-like appearance (Fig 2, A). The nidus stage was defined as the tortuous arteriovenous components (Fig 2, B) and the absence of a dilated vein. The venous phase occurred relatively late. During the venous phase, the contrast gradually flowed into the dilated outflow vein. The DOV was identified in this phase as an obviously dilated outflow vein in the venous phase of selective angiograms. The tortuous part of the nidus and DOV were observed on all the angiograms (Fig 2, C).
Fig 2.
Angiography of the femoral artery showing feeding artery (arrows) in the arterial phase (A), tortuous arteriovenous components (arrow) in the nidus phase (B), and a dilated dominant outflow vein (DOV; arrows) in the venous phase (C).
Treating the DOV and nidus
After the DOV was identified, a 17.8-guage needle (Cook Medical Inc, Bloomington, IN) was used to percutaneously puncture the DOV under roadmap guidance. After verifying the location of the needle in the DOV using the venogram (Fig 3, A), a 2.2F microcatheter (Asahi, Seto, Japan) was inserted through the needle into the dilated venous sac (Fig 3, B). Guided by the guidewire, the microcatheter was first introduced to the proximal end of the DOV, which was close to the deep vein, and gradually withdrawn. The coils were released along the DOV to the distal end of the DOV, which was close to the nidus.
Fig 3.
A, Dominant outflow vein (DOV) venogram from direct puncture showing the degree of dilation and direction of the reflux vein (arrows). B, A 2.2F microcatheter (arrow) was introduced into the DOV through the needle, and coils were released to occlude the outflow vein. C, Venogram from the puncture needle showing an obvious reduction in outflow from the vein and contrast stain.
DOV occlusion with coils
After confirming that the microcatheter was positioned correctly, three-dimensional (3D) detachable coils (Interlock; Boston Scientific, Marlborough, MA) were inserted through the microcatheter (Fig 3, C). During insertion of the detachable coils, the surgeon applied external pressure to the proximal end of the DOV manually using a finger. This pressure stimulated 3D coil pattern formation, reducing the risk of coil migration. Nester coils (Cook Medical Inc) were released after obliteration of the distal end of the draining veins to create a compact DOV obliteration. When the venogram revealed a significant reduction in the outflow and clear contrast staining, coil insertion was stopped (Fig 3, C). The size, type, and number of coils were recorded in all cases.
Eradication of nidus with absolute ethanol
After DOV embolization, contrast medium was injected into the proximal end of the coils. With obstruction by the coils, the contrast medium streamed back into the vascular mass, where the nidus was located. DOV embolization slowed the blood flow, resulting in clearer identification of the nidus. Absolute ethanol was injected through the needle into the nidus. Several venograms via the needle or microcatheter were performed before absolute ethanol injection into the nidus to determine the volume and rate per injection. The contrast medium should only be visible in the nidus and draining veins and not in the feeding arteries. Angiography of the feeding arteries was performed 3 to 5 minutes after ethanol injection to determine whether the nidus had been embolized. The arterial and venous phases of angiography were carefully observed to determine whether the ethanol injection should be repeated (Fig 4).
Fig 4.
Angiography of the femoral artery performed after ethanol embolization showing complete obliteration of the arteriovenous malformation (AVM) in both the arterial phase (before embolization [A]; after embolization [B]) and the venous phase (before embolization [C]; after embolization [D]).
Postoperative management
After embolization, all 12 patients were given intravenous methylprednisolone for 3 to 5 days to relieve swelling and ranitidine to prevent the development of gastric or duodenal ulcers.
Clinical evaluation and follow-up
Follow-up was conducted at 1- to 3-month intervals after the initial treatment. Contrast-enhanced computed tomography or angiography was recommended if the patient's clinical symptoms and signs worsened. If AVMs were still observed or the clinical symptoms persisted, additional embolotherapy was required. For patients with a complete response to treatment, a telephone questionnaire was administered every 3 months, and a physical examination was performed every 1 year. Angiography was performed at least once 1 year after the last embolization session for observation for all our patients with a complete response. The devascularization rate was determined from the last angiogram during follow-up compared with the baseline angiogram.
The therapeutic response to ethanol embolization was analyzed by two radiologists according to the degree of AVM disconnection shown before and after embolization. The clinical outcomes (ie, complete resolution, improvement, no change, aggravation) and complications were evaluated by a surgeon and an interventional radiologist by assessing the patients’ signs and symptoms.
The evaluation of the clinical symptoms and signs was divided into the following 4-point grading scale: 1 point, aggravated AVM lesions or increased pain or complications, regardless of the degree of devascularization on angiography; 2 points (no response), an AVM resolution rate of ≤49%; 3 points (partial response), complete resolution or improvement in the clinical symptoms and signs, with 50% to 99% devascularization of the AVMs; and 4 points (complete response), complete resolution of the clinical symptoms or 100% angiographic devascularization on arteriography after >12 months of follow-up (Fig 3, D). Partial and complete responses were considered effective treatment outcomes. The standards of the Society of Interventional Radiology classification were used to determine whether the complications were classified as major or minor.8
Results
A total of 20 coil-assisted DOV occlusions were performed with 27 3D detachable coils (0.018-in.; Interlock; Boston Scientific) and 139 3D Nester coils (0.018-in., Cook Medical Inc; Table II). No complications related to DOV occlusion with coils were observed in any patient.
Table II.
Results of ethanol embolization and coil occlusion of dominant outflow veins (DOVs) in arteriovenous malformation (AVM) in lower extremities
| Pt. No. | Embolization procedures, No. | Coils, no. |
Ethanol volume,c mL | Clinical follow-up, months | Clinical outcome | |
|---|---|---|---|---|---|---|
| Detachablea | Undetachableb | |||||
| 1 | 3 | 2 | 20 | 15; 15; 5 | 26 | PR |
| 2 | 1 | 1 | 12 | 3 | 25 | CR |
| 3 | 4 | 6 | 28 | 12; 6; 16; 6 | 22 | PR |
| 4 | 2 | 3 | 16 | 8; 5 | 29 | PR |
| 5 | 2 | 1 | 7 | 8; 4 | 18 | CR |
| 6 | 3 | 2 | 17 | 18; 5; 5 | 25 | CR |
| 7 | 1 | 1 | 3 | 9 | 14 | CR |
| 8 | 3 | 1 | 6 | 12; 6; 6 | 16 | CR |
| 9 | 3 | 4 | 22 | 11; 8; 12 | 26 | PR |
| 10 | 2 | 1 | 8 | 8; 6 | 32 | PR |
| 11 | 3 | 4 | 22 | 11; 8; 12 | 36 | CR |
| 12 | 2 | 1 | 8 | 8; 6 | 37 | CR |
AVM, Arteriovenous malformation; CR, complete response; PR, partial response; Pt. No., patient number.
Three-dimensional coils (Interlock; Boston Scientific, Marlborough MA) 20 mm in unconstrained diameter and 40 cm in stretched length.
Three-dimensional 0.018-in. Nester coils (Cook Medical Inc, Bloomington, IN) 8 mm in unconstrained diameter and 14 cm in stretched length.
Some patients had >1 session of ethanol administration.
A total of 29 ethanol embolization procedures (mean, 2.4; range, 1-4) were performed in the 12 patients with an average ethanol volume of 8.8 mL per procedure (range, 3.0-18 mL). The angiographic results showed that 100% AVM devascularization was achieved in seven cases (58.3%) and 76% to 99% AVM devascularization was achieved in five (41.7%). Ethanol embolization combined with coil-assisted DOV occlusion achieved effective therapeutic outcomes in all patients (Table II). Seven of the 12 patients (58.3%) achieved a complete response with no recurrence found by imaging studies and/or clinical follow-up. Five patients (41.7%) showed partial resolution of the clinical signs and symptoms.
Complications
During the study, no major complications were observed. All 12 patients (100%) developed focal swelling immediately after the procedure, which had been significantly relieved within 3 to 5 days. Three patients (25%) experienced blister and skin ulcers at the lesion site, which had healed spontaneously within 1 to 3 weeks without any remaining tissue defects.
Discussion
AVMs are among the most challenging enigmas in medicine. Because of its low incidence rate, it is difficult for a radiologist to diagnose and optimally manage these malformations. An understanding of the hemodynamics and angioarchitecture is the basis for the treatment of AVMs. Thus, the recurrence and aggravation of lesions after ligation or embolization of feeding arteries often occur.2,9,10 The key to curing AVMs is isolation and interruption of the actual site of communication between the artery and vein, where the nidus is located.11, 12, 13 We successfully treated 12 patients with AVMs with a DOV by eradicating the nidus and discussed the methods used to identify, reach, and eradicate the nidus.
It is critical to accurately define the severity and extent of AVMs to select the appropriate treatment. The initial step in managing AVMs with a DOV is to perform pretreatment imaging examinations. Advances in imaging have allowed us to better understand the angioarchitecture of the nidus to optimize treatment and minimize the risk of endovascular therapy. The four minimally invasive imaging modalities currently used to visualize AVMs before treatment are ultrasound, magnetic resonance angiography, computed tomography angiography, and catheter angiography. DSA is the best tool available to define the arterial supply to the lesion, presence of a nidus, size of the arteriovenous shunting, and venous drainage, especially for treatment considerations.5,14,15 Doppman3 used DSA to identify the nidus as described in the Methods section, and the nidus was observed during the nidus phase of angiography. The nidus phase is a transitional phase between the arterial and venous phases. The nidus revealed a complex vascular network consisting of arterial and venous components.3 Contrast can be streamed backward to the nidus close to the DOV during venography from the tip of the microcatheter or puncture needle after DOV embolization using coils, allowing for easier nidus identification, as shown in our results.
For arteriovenous fistulas, the catheter can be inserted transarterially into the fistula or outflow vein. There are primarily three approaches to access the nidus of AVMs with multiple feeding arteries and outflow veins and a nidus: transarterial, transvenous, and direct percutaneous approaches. The feeding arteries can be severely tortuous, making transarterial approaches difficult. The complicated angioarchitecture of certain types of AVMs, in which multiple arterioles shunt into the outflow vein, can also make reaching the nidus using the transarterial approach difficult.1,11,12,16,17 During transarterial embolization, stimulating ethanol or other agents have a high probability of embolizing or causing vasospasm in the proximal section of the feeding artery. This results in a phenomenon similar to proximal ligation of a feeding artery of an AVM, which could worsen the clinical condition by recruiting collateral arterial feeders. Direct puncture of the nidus or transvenous embolization using coils could achieve better results because the outflow vein will generally be visibly dilated compared with the feeding arteries, making direct puncture into the nidus of the outflow vein feasible.18,19 With guidewire guidance, the microcatheter inserted through the needle can be easily introduced into the proximal end of the outflow vein and gradually withdrawn while the coils are released to block the DOV.
Although numerous liquid embolization agents have been used for the treatment of AVMs, they do not cause the destruction of AVM endothelial cells. Chronic inflammatory and hypoxic conditions after incomplete embolization are associated with repeat endothelialization and recanalization of AVMs.20, 21, 22 Absolute ethanol causes apoptosis and necrosis of the endothelial cells, which results in vascular wall fractures. However, anhydrous ethanol, as the most effective embolization agent, does not guarantee a successful outcome for all extracranial AVMs. For AVMs with distinct venous sacs, the administered ethanol can be diluted by blood and carried away before nidus occlusion. Therefore, coils are needed to reduce the nidus volume and flow before administration of ethanol.23, 24, 25, 26 Using coils to reduce the volume of the nidus, AVMs can be treated with fewer sessions and less ethanol. The primary embolization agents for the treatment of AVMs with DOV were the combination of absolute ethanol and coils.
In brief, DOV embolization has the following several benefits. First, DOV embolization slowed the blood flow, which made nidus identification clearer. Second, DOV embolization slowed the blood flow, which made it easier to destroy with a limited amount of absolute ethanol. Finally, in the long term, DOV embolization might reduce the possibility of recurrence of AVMs.
Conclusions
Treatment of lower extremity AVMs with a DOV is one of the most challenging clinical issues. Nidus identification and the selection of appropriate embolic agents provide a potential solution with acceptable complications. Staged and precise ethanol embolization shows promising safety and efficacy. The proper use of coils to occlude the DOV is necessary.
Author contributions
Conception and design: LS, XY, DW
Analysis and interpretation: LS, ZW, MW, XF, DW
Data collection: LS, XY, ZW, MW
Writing the article: LS, XY, ZW, MW, XF
Critical revision of the article: LS, DW
Final approval of the article: LS, XY, ZW, MW, XF, DW
Statistical analysis: Not applicable
Obtained funding: LS
Overall responsibility: LS
LS and XY contributed equally to this article and share co-first authorship.
Footnotes
The present study was supported by the Health Clinical Research Project of Shanghai Municipal Health Commission (grant 202140425) and Clinical Research Program of Ninth People's Hospital, Shanghai Jiaotong University School of Medicine (grant LYLJ201911).
Author conflict of interest: none.
The editors and reviewers of this article have no relevant financial relationships to disclose per the Journal policy that requires reviewers to decline review of any manuscript for which they may have a conflict of interest.
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