Leg ulcer due to multiple arteriovenous malformations in the lower extremity of an elderly patient

Abstract

A 66‐year‐old woman with a history of deep vein thrombosis (DVT) presented with an irregularly shaped leg ulcer surrounded by pigmentation on the left lower limb. In addition, the circumference of her left thigh had gradually increased. The ulcer did not respond to topical treatment and enlarged, therefore, she visited our hospital. Arteriography of the left lower limb showed multiple arteriovenous malformations (AVMs), based on which we made a diagnosis of a leg ulcer due to multiple AVMs. Transcatheter arterial embolisation with a mixture of N‐butyl‐2‐cyanoacrylate and lipiodol was performed six times in the period of about a year for treating the AVMs. The ulcer was managed with bed rest, surgical debridement, continuous pressure support with elastic wrap and topical treatment. After 15 months, the ulcer healed, leaving pigmentation and scarring. It is quite rare for AVMs to progress in the elderly. We speculate that the DVT had caused occult AVMs to become symptomatic following an increase in size.

Introduction

Arteriovenous malformations (AVMs) can result in dermatological manifestations, such as a reddish, eczematous reaction, angiodermatitis 1, 2, ulcerations and nodules which have been reported as pseudo‐Kaposi's sarcoma 3. Some cases result in life‐threatening congestive heart failure or even intractable bleeding. If the AVMs are excised, the skin ulcer may be cured; however, many cases of AVMs are difficult to excise. Here, we report a case of a leg ulcer due to multiple AVMs along the internal/external iliac artery and its branches that continue to the dorsal artery of the foot.

Case report

A 66‐year‐old woman had a history of swelling of her left lower limb associated with deep vein thrombosis (DVT) of the left femoral and popliteal vein in 2004 and had been commenced on warfarin. Placement of an inferior vena cava filter had not been performed. The circumference of her left thigh gradually increased to 50 cm in September 2005, compared with the circumference of 36 cm of her right thigh. An ulcer appeared on the anterior aspect of her left leg in July 2006 without a history of trauma, and the circumference expanded to 71 cm. The ulcer did not respond to topical treatment and enlarged. When we examined her for the first time in April 2007, there was an ulcer with dimensions of 20 × 25 cm² on the anterior aspect of her lower left leg with an irregular border and hyperpigmentation (Figure 1A). The ulcer base had yellowish necrotic tissue. Dilated superficial veins and capillary malformation were not found on the skin surface. The left thigh was warmer than the right thigh.

Figure 1.

An ulcer with irregular borders and hyperpigmentation on her left leg in April 2007 (A). The ulcer healed 15 months later (B).

Her blood test revealed anaemia with a haemoglobin level of 7·9 g/dl, C‐reactive protein 5·02 mg/dl and D‐dimer level of 1·00 µg/dl. The prothrombin time‐international normalized ratio (PT‐INR) was 2·44. Other laboratory data, including haematology, serum biochemistry, liver function and renal function were within normal limits. She tested negative for antiphospholipid antibodies. Bacteriological culture of the discharge from the ulcer showed Pseudomonas aeruginosa. Chest roentgenogram showed mild heart enlargement suggestive of chronic heart failure. Ankle brachial pressure index (ABPI) of the right and left sides was 1·14 and 1·16, respectively. Histologic examination of a skin biopsy from the border of the leg ulcer showed proliferation of irregularly shaped blood vessels, fibroblasts, extravasation of red blood cells, and haemosiderin deposits in the dermis. These were non‐specific features seen in stasis ulcers, without evidence. Thermography (Handy Thermo TVS‐200^®, NEC Avio, Tokyo Japan) of the lower limbs revealed that the left lower limb was about 3°C warmer than the right lower limb (Figure 2A). Computed tomographic angiography and magnetic resonance angiography demonstrated enhanced vessels suggestive of multiple vascular malformations (Figure 2B). The left femoral bone did not appear longer and larger than the right femoral bone. Angiography revealed multiple, enlarged, mesh‐like, high‐flow vascular malformations in different independent locations along the arteries supplying the left leg, involving the internal/external iliac arteries and its branches that continue to the dorsal artery of the foot. These findings were suggestive of AVM, including a few arteriovenous fistulas (AVFs) (Figure 3A, B). On the basis of the above findings, the diagnosis of a leg ulcer due to multiple AVMs was made.

Figure 2.

Thermography revealed that the left lower limb was about 3°C warmer than the right lower limb (A). Computed tomographic angiography demonstrated enhanced vessels suggestive of multiple vascular malformations of the left lower limb (B).

Figure 3.

Angiography revealed multiple, enlarged, mesh‐like lesions of vascular hyperplasia along the arteries supplying the left leg, involving the internal/external iliac arteries and its branches that continue to the dorsal artery of the foot. The left iliac artery flows into the vein on the right side through a varix (▾) (A, B). AVMs were either reduced in size or completely obliterated after five TAEs (C).

As it was difficult to treat the extensive AVMs by excision, sclerotherapy or radiation therapy, transcatheter arterial embolisation (TAE) with a mixture of N‐butyl‐2‐cyanoacrylate (NBCA) and lipiodol was performed six times at 1‐ to 2‐month intervals during the period of 1 year, resulting in a gradual reduction of the AVMs that was confirmed by angiography. We mixed NBCA with lipiodol at ratios of 1:1·25–1:10, using a total of 3 ml of NBCA and 10 ml of lipiodol. The approach was from the arterial side. Six sessions of TAE were performed to reduce the risk of ischaemia and to increase the effectiveness of the TAE. After treatment, the AVMs were either reduced in size or completely obliterated (Figure 3C). In addition, the ulcer was managed conservatively with bed rest, surgical debridement, continuous pressure support with elastic wrap (L‐Weave^®, Nippon Sigmax, Tokyo Japan) and topical treatment. After 15 months, the ulcer of her left leg healed, leaving pigmentation (Figure 1B).

Discussion

AVMs are defined by high‐flow lesions of vascular malformations. Vascular anomalies are classified into haemangiomas and vascular malformations 4. Vascular malformations arise from aberrant vessel angiogenesis and comprise direct microscopic connections between arteries, veins and lymphatic vessels without a normal capillary bed. They are divided into low‐flow or high‐flow lesions based on their haemodynamic flow characteristics. AVMs and AVFs, which are vascular malformations with an arterial component, are classified as high‐flow lesions. AVMs have a nidus – abnormal channels connecting the arteries and veins – whereas AVFs do not have a nidus. Some vascular malformations appear as part of a familial genetic disorder. Parkes Weber syndrome is a condition characterised by nevus flammeus and AVMs associated with hypertrophy of the soft tissues or bones of the extremities 5, features of which were absent in this case apart from the AVMs.

It is rare for AVMs to progress from stage 1 to stage 3 in the elderly. AVMs are congenital lesions and do not regress 6. Approximately half are noticeable in the neonatal period, and many others become apparent during childhood 7. AVMs may be classified into four stages using the Schobinger classification 8: stage 1 is characterised by macular lesions, pink patches or warmth; stage 2 is characterised by a mass with a bruit and thrill, changes of which may mimic Kaposi's sarcoma in adults; stage 3 is characterised by ulceration, pain or haemorrhage and stage 4 is associated with cardiac compromise from increased preload. It has been suggested that some cases of AVMs grow and change from stage 1 to stage 2 because of vascular engorgement resulting from trauma, infection or hormonal fluctuations during pregnancy and puberty 9.

Interestingly, the skin ulcer and other left limb symptoms in this case were absent prior to 2004, and the left popliteal vein showed no high flow on initial assessment in 2005 (Figure 4A) but had high flow with an arterial component 4 years later (Figure 4B) on Doppler ultrasonography. These observations suggest that the AVMs gradually grew from 2004. We postulate that AVMs may be affected by the presence of thrombosis. Similar to our case, Chikamatsu et al. reported a case of an elderly patient with congenital pelvic AVMs who developed iliac vein thrombosis 10. In that report, the authors formulated a hypothesis to explain why the congenital AVMs were complicated by iliac vein obstruction. They hypothesised that obstruction of the iliac vein increased venous blood pressure. Therefore, it is possible that thrombosis causes the AVM to increase in size, similar to our hypothesis.

Figure 4.

Doppler ultrasonography. In 2005, the left popliteal vein had no high flow (A), but it had high flow with an arterial component 4 years later (B). The flow direction was antegrade, not retrograde. The probe was directed opposite to the direction of the blood flow.

In this case, two factors contributed to the leg ulcer. One is the steal phenomenon. There was arterial ischaemia due to the steal phenomenon involving the AVMs in the leg. The second factor was venous hypertension due to the AVMs in the proximal side of the left lower limb. The stasis of the skin microcirculation was related to the venous hypertension.

Postthrombotic syndrome (PTS) may occur as a complication of DVT 11. It has been reported that 20–50% patients with DVT have PTS within 1–2 years of DVT onset. Clinical manifestations of PTS include heaviness, pain, itching, swelling and ulceration (Table 1). Some of these symptoms were present in our case. Although we cannot rule out the possibility of PTS, PTS cannot explain the significant enlargement of the AVMs and the effectiveness of TAE therapy.

Table 1.

Comparison of postthrombotic syndrome and the clinical consequences of AVM in lower limb

	Postthrombotic syndrome	AVM in lower limb
History	Complication of DVT	Congenital
Frequency	20–50% patients with DVT	Rare
Clinical features	Heaviness, pain, swelling, itching, stasis dermatitis (eczema), reddish, hyperpigmentation, telangiectasia, venous dilation, ulceration	Warmth, palpable thrill, audible bruit, swelling, limb enlargement, itching, eczema, pain, reddish, hyperpigmentation, ulceration, bleeding, angiodermatitis, pseudo‐Kaposi's sarcoma
Diagnosis	No gold standard test; Doppler ultrasound	Angiography, Doppler ultrasound, CTA, MRA
Treatment	Elastic compression stocking, intermittent compression extremity pump	Excision, embolisation, sclerotherapy, embolosclerotherapy, radiation therapy
Prognosis	Usually good	More problematic, heart failure, cutaneous ischaemia, limb amputation

AVM, arteriovenous malformation; CTA, computed tomographic angiography; DVT, deep vein thrombosis; MRA, magnetic resonance angiography.

Despite many published reports, the optimal treatment for AVMs is not well established. The basic aim of treatment is to remove the nidus and obliterate the malformation. Small AVMs may be resected and reconstructed 6. However, complication rates for surgery are high; Upton et al. reported a complication rate of 28% in 33 cases of high‐flow lesions 12. Large AVMs may be managed by embolisation 13, 14, sclerotherapy, radiation therapy, and, as a last resort, amputation. Embolisation may provide symptom relief and downgrade the Schobinger status. However, inadequate treatment may result in recurrence that is more problematic than the initial lesion. Therefore, a combined approach is beneficial 7, 15, as reflected by the increasing use of embolosclerotherapy in the treatment of limb AVMs. Embolosclerotherapy is a treatment method involving transarterial embolisation followed by sclerotherapy. Nevertheless, failure and complication rates are high; Lee et al. reported a complication rate of 31·3% in 99 cases of vascular malformations 16. Radiation therapy is reportedly effective 17, but further confirmation of its efficacy and assessment of the possibility of radiation‐induced malignancy is required. In our case, we selected embolisation because the patient had multiple AVMs involving the iliac artery and its branches that supply the dorsal artery of the foot, which made it difficult to excise or apply sclerotherapy or radiation therapy. Embolisation decreased venous pressure and was useful in alleviating the congestive symptoms in the lower limb. Bed rest and continuous pressure support with elastic wrap were helpful in the treatment of the leg ulcer.

In conclusion, we report a case of a leg ulcer due to multiple AVMs of the left lower extremity. It is rare for AVMs to enlarge in the elderly. We speculate that the AVMs may have been affected by the presence of DVT. Unilateral limb swelling, increased warmth and chronic ulceration were suggestive of the presence of AVMs.