Steal phenomenon in the lower limb: presentation of a case with osseous metastases secondary to renal cell carcinoma and review of the literature

Abstract

Renal cell carcinoma is reported to have potent angiogenic activity with a high microvascular density in both primary and metastatic sites compared with other adenocarcinomas. Angiogenesis can lead to the formation of abnormal arteriovenous shunts that can, in patients with peripheral vascular disease, result in worsening of the degree of ischaemia by producing a vascular steal-like phenomena. Nevertheless, steal phenomena secondary to malignancies are extremely rare. We report a case of distal critical limb ischaemia in a patient with peripheral vascular disease exacerbated by massive arteriovenous shunting due to tibial metastases from renal cell carcinoma.

BACKGROUND

Renal cell carcinoma (RCC) accounts for 2% of all cancers worldwide, with an annual incidence of 1.5–6%.^1,2 Overt metastases are found in 30–60% of patients at presentation with the lungs being the commonest site.³ Bony secondaries develop in one-third of patients.^4,5 Neovascularisation in association with osseous metastases has been described sparsely in the literature⁶ as is the process of arteriovenous (AV) shunting resulting from abnormal tumour circulation. In our case we describe a case of a steal-like phenomenon in the lower limb of an elderly patient where peripheral vascular disease is exacerbated by AV shunting resulting from osseous tumour metastases with a comprehensive review of the relevant literature.

CASE PRESENTATION

An elderly man presented with critical ischaemia of the left foot for 12 months with dry gangrene of the first and second toes. He had a history of peripheral vascular disease causing intermittent claudication in both legs for 4 years. He had also had RCC of the right kidney for a similar duration. As he declined any urological intervention, his renal cancer was followed up regularly by abdominal ultrasonography and chest x-ray. During follow-up, his cancer progressed and he developed a secondary deposit in his right suprarenal gland. No other distant metastases were detected until the time of admission. He had other significant co-morbidities, including peptic ulcer disease, ischaemic heart disease and a pacemaker for symptomatic bradycardia.

Physical examination revealed dry gangrene of the first and second toes with extension to the medial aspect of the left foot. Pulses were absent bilaterally below the level of femoral arteries, except for a diminished right popliteal pulse. There were visible varicose veins as well as a moderate-sized swelling in the left calf.

Endovascular treatment, in the form of angioplasty of the popliteal and tibial occlusions of the left leg, combined with embolisation of the tibial metastases was considered; however, the patient declined further intervention. Over the following 2 months his foot ischaemia and general condition deteriorated culminating in sepsis and death shortly after.

INVESTIGATIONS

Doppler ultrasound confirmed the varicosities and excluded the presence of deep vein thrombosis. The working diagnosis was critical ischaemia due to peripheral vascular disease and re-vascularisation was planned. Arteriography revealed a vascular right renal tumour and patent pelvic vessels. In the asymptomatic right leg there was evidence of severe atherosclerotic disease with a tight stenosis of the profunda femoris artery and severe stenotic disease of the popliteal artery. All three tibial and peroneal arteries were occluded proximally but the latter was filled distally by collateral circulation. In the critically ischaemic left leg there was a 3 cm occlusion of the superficial femoral artery in the adductor canal, and diffuse disease of the popliteal artery with complete occlusion at the level of the knee. The posterior tibial artery was patent with extensive collateral circulation at the level of the mid-calf. An abnormal tumour circulation was also noted on the arterial phase in the tibia where large lytic bony deposits were seen (figs 1–3). Extensive AV shunting through the tumour circulation resulted in a significant reduction of blood flow to the leg and foot distally.

Figure 1.

Radiograph showing extensive lytic destruction of left tibial shaft consistent with metastatic disease (arrows).

Figure 2.

Digital subtraction in early arterial phase showing occlusive atheromatous disease with collateral filling of left posterior tibial and peroneal arteries (long arrows). There is tumour staining in the tibial shaft (short arrow).

Figure 3.

Angiographic image 1.5 s later showing arteriovenous shunting (S) with rapid filling of the posterior tibial and popliteal veins (arrows).

OUTCOME AND FOLLOW-UP

Endovascular treatment, in the form of angioplasty of popliteal and tibial occlusions of the left leg, combined with embolisation of the tibial metastases was considered; however, the patient declined further intervention. Over the following 2 months his foot ischaemia and general condition deteriorated culminating in sepsis and death shortly after.

DISCUSSION

RCC accounts for 2% of all cancers worldwide, with an annual incidence of 1.5–6%.^1,2 Overt metastases are found in 30–60% of patients at presentation with the lungs being the commonest site.³ Bony secondaries develop in one-third of patients.⁴ Most of these are in the axial skeleton, with a small percentage in the long bones. The incidence of tibial metastasis is reported to be about 1.3–3%.^4,5 Bony secondaries commonly present with skeletal pain (75%), long bone fractures (42%), hypercalcaemia of malignancy (29%) and spinal cord compression (13%).^3,4

Arterial steal phenomenon refers to the shunting of blood flow from an artery with higher resistance (due to a stenosis or occlusion) to another blood vessel with lower resistance.⁷ This results in diminution or reversal of blood flow in the diseased artery distal to the occlusion, and can potentially lead to ischaemia.⁸ Contorni⁹ first described it in the vertebral artery in association with occlusive disease of subclavian artery. Other commonly reported sites include the coronary and CNS circulation, and iatrogenic AV fistulae in haemodialysis.^10–12 Steal phenomenon has rarely been described in association with metastatic RCC.¹³

Among all adenocarcinomas, RCC has the highest vasogenic potential and microvascular density at both the primary and secondary sites.⁶ Abnormal AV shunts within this vascular meshwork provide a rich blood supply to the tumour deposits.¹⁴ The clinical presentation of malignant AV shunting caused by osseous metastasis is not well described in the literature, but has been reported as pulsatile tumours in the sternum¹⁵ and proximal tibia.¹⁶ Howlett and Caranasos¹³ reported a case of RCC secondaries in the patella and iliac bones generating extensive AV shunting and lower limb ischaemia. Osseous RCC metastasis presenting as deep venous thrombosis has also been described.¹⁷

The present patient was known to have severe bilateral PVD that could be argued to be the underlying cause of his critical ischaemia. In addition to his arterial disease, however, there were numerous AV shunts within the metastatic deposit creating a tumour “steal” phenomenon.

Targeting the secondary tumour circulation might contribute to treatment of distal ischaemia in this setting. Different treatment approaches for osseous metastasis in RCC have been proposed. The majority (81%) receive radiotherapy, while one-third undergo amputation or limb salvage surgery. While radiotherapy has been reported to have a satisfactory outcome in reducing skeletal complications, it might not be feasible in the context of chronic ischaemia as it may have a detrimental effect on the peripheral circulation. Other more appropriate treatment options that are used for advanced RCC include cytokine-based immunotherapy.³ Nevertheless, several limitations exist including low success rate, systemic side-effects and low cost-effectiveness.¹⁸

Vallence et al¹⁹ reported spontaneous AV fistula formation in association with PVD in three patients. Symptoms settled after successful treatment of the AV fistulae with percutaneous angioplasty in one case and bypass grafting in the other two.

Embolisation of metastasis circulation has been used in RCC as a preoperative adjunct to surgery²⁰ and in the palliative treatment of bone pain,²¹ and would have been the preferred option in this patient had he not declined treatment.

LEARNING POINTS

• Peripheral limb ischaemia can be exacerbated by tumour metastasis from RCC.

• This was most likely due to a steal-like phenomenon leading to further deterioration of an already ischaemic limb.

• The best treatment in this setting is currently unknown, but embolisation of the tumour circulation with or without re-vascularisation is the most attractive option.