A Case of Brachial Artery Thrombosis Caused by Massage of an Occluded Arteriovenous Graft

: Background: Acute upper limb ischemia (AULI) is a potential complication associated with massages of occluded vascular accesses in patients undergoing hemodialysis. Pharmacological thrombolysis, endovascular intervention and surgical intervention are possible treatment options. Deciding the appropriate treatment strategy is still a controversial issue. Case Presentation: The patient was a 43-year-old woman with renal failure who underwent hemodialysis and peritoneal dialysis. She was found to have an arteriovenous graft (AVG) thrombosis at the start of a hemodialysis session. She underwent massage of the vascular access, and immediately after the massage, she reported pain and cyanosis in her right-hand ﬁngers and was referred to our hospital. Duplex ultrasonography revealed a large number of thrombi in the brachial, radial and ulnar arteries. AULI due to brachial artery thrombosis was diagnosed and surgical intervention was performed on the same day. The vascular wall of the forearm artery was incised vertically against the running vessel, and thrombi around the bifurcation of the radial and ulnar arteries were removed. Angiography guided-surgical intervention was performed and improvement in blood ﬂow was achieved. The patient was discharged on the second day after the operation. Conclusion: Surgical intervention has been reported as an effective treatment of AULI due to brachial artery thrombosis after massage of an occluded vascular access.


Introduction
Vascular access in hemodialysis patients can cause a thrombotic occlusion due to blood pressure reduction, dehydration and venous stenosis [1]. In these cases, both endovascular intervention and surgical intervention may be employed as therapeutic procedures [2]. As an early treatment option, massage of the occluded vascular access may be performed to break thrombi and to disperse them. However, if a coarse thrombus disperses to a central or peripheral site, secondary complications may occur [3]. Furthermore, there is scant evidence for the safety and efficacy of massages. Treatment strategies for AULI, one of the possible massage complications, include thrombolytic therapy, endovascular intervention and surgical intervention [4], but many aspects of the treatment planning and decision making are determined by the practical capabilities and local availability of each facility [5]. Here, we report a case of successful surgical intervention for AULI occurred after massage of an occluded vascular access for dialysis.

Case Report
The patient was a 42-year-old woman with lupus nephritis who started hemodialysis after renal failure occurred in 2011. During the hemodialysis treatment, she experienced repeated thrombotic occlusions and consequently underwent several endovascular interventions, surgical interventions and revascularization. In 2017, peritoneal dialysis combined with weekly hemodialysis was started, and in 2018 an expanded polytetrafluoroethylene (ePTFE) graft between the brachial artery and basilic vein was inserted into the right forearm; however, thrombotic occlusions recurred. Blood tests showed no abnormalities in anti-phospholipid antibody profile or in the coagulation system. In 2019, at routine control pre-hemodialysis, arterio venous graft (AVG) flow was not detected: consequently an AVG occlusion was suspected. Despite the administration of urokinase (60,000 units), following which a vascular massage was performed, reperfusion was not achieved. Immediately after the massage, the patient suffered from pain and exhibited cyanotic discoloration in the right distal forearm and was referred to our hospital for examination and treatment. Vital signs were preserved at the first visit. The patient's right hand fingers, 2nd to 4th, exhibited a violet coloration of the distal phalange and were cold to touch, and painful ( Figure 1). No sensory or motor deficit was observed at this level. Pulse was absent in the radial artery and feeble in the ulnar artery at palpation. B-mode ultrasonography revealed extensive luminal thrombi, ranging from the arterial anastomotic site to the arteries of the forearm, involving some traits of the ulnar artery and distally in the radial artery. Duplex ultrasonography confirmed the absence of blood flow in the forearm arteries. The patient was diagnosed with AULI due to thrombotic reflux and underwent surgical intervention on the same day.
Kidney Dial. 2021, 1, FOR PEER REVIEW 2 was initiated, and in 2018 an expanded polytetrafluoroethylene (ePTFE) graft between the brachial artery and basilic vein was inserted into the right forearm; however, thrombotic occlusions recurred. Blood tests showed no abnormalities in the anti-cardiolipin antibody or the coagulation system. In 2019, AVG flow was not detected before hemodialysis at the previous clinic, and an AVG occlusion was suspected. After the administration of urokinase (60,000 units), a shunt massage was performed, but reperfusion was not achieved. Immediately after the shunt massage, the patient suffered pain and cyanosis in the right peripheral forearm and was referred to our hospital for examination and treatment. No abnormal vital signs were detected at the first visit. The patient had coldness and pain in the right peripheral second to fourth fingers, with violet-colored skin ( Figure 1). No movement or perceptual disorder was found. Pulsation was absent in the radial artery and feeble in the ulnar artery on palpation. Luminal thrombi were found extensively during Bmode ultrasonography, from the arterial anastomotic site to the forearm artery, some parts of the ulnar artery, and the peripheral radial artery. Duplex ultrasonography confirmed the absence of blood flow in the forearm artery. The patient was diagnosed with AULI due to thrombotic reflux and underwent surgical intervention on the same day. A skin incision was made just above the arteriovenous anastomosis, parallel to the blood vessel, in the area of the brachial artery thrombus ( Figure 2). The vascular wall was incised vertically along the vessel direction by hooking the central artery with a bulldog clamp; however, bleeding did not occur. Arterial thrombi near the incised sites were removed using a 3-Fr Fogarty catheter, mosquito forceps, and tweezers. Angiography performed during surgery still failed to detect blood flow in the radial artery, and we suspected that thrombi might have remained in the peripheral radial artery (Figure 3a). Therefore, additional thrombectomy was performed in the radial artery and a long single thrombus was removed (Figure 3b). Angiography performed again showed improved blood flow in the radial artery. The surgery was completed after pulsation in the radial and ulnar arteries was confirmed by palpating the wrist. The operative time was 1 h and 12 min. A skin incision was made just above the arteriovenous anastomosis, parallel to the blood vessel, in the area of the brachial artery thrombus (Figure 2). The vascular wall was incised vertically along the vessel direction by hooking the central artery with a bulldog clamp; bleeding did not occur. Arterial thrombi near the incised sites were removed using a 3-Fr Fogarty catheter, mosquito forceps and tweezers. Angiography performed during surgery failed to detect blood flow in the radial artery, therefore we hypothesized that thrombi might have involved the peripheral radial artery (Figure 3a). Therefore, additional thrombectomy was performed in the radial artery and a long single thrombus was removed (Figure 3b). Angiography was re-performed, showing improved blood flow in the radial artery. The surgery was completed after radial and ulnar pulses were found to be detectable at the wrist. The full procedure took 1 h and 12 min.
Immediately after surgery, the color of the fingers improved. Heparin at 500 unit/hour was infused intravenously after surgery. Hemodialysis resumed on the first day after surgery and no thrombus was found in intravascular spaces two days after surgery by duplex ultrasonography. The patient was discharged from hospital on the same day of the procedure.
Immediately after surgery, the color of the fingers improved. Heparin at 500 unit/hour was infused intravenously after surgery. Hemodialysis resumed on the day after surgery, and no thrombus was found in intravascular spaces two days after surgery by duplex ultrasonography. The patient was discharged from hospital on the same day.

Discussion
Endovascular intervention and surgical intervention are recommended as treatments for the occlusion of vascular access [6,7]. On the other hand, none of the guidelines recommend or oppose massage as an immediate treatment for vascular access thrombosis. In clinical practice, a shunt massage is a procedure to break thrombi by external physical stimulation and disperse them to a central area [3]. The benefit of this procedure is that it can be performed immediately after a thrombotic occlusion occurs. At the same time, a risk associated with the procedure is that the dispersal of a coarse thrombus to a central site may lead to the development of a pulmonary embolism [8], whereas thrombi dispersing to the periphery represent a risk of brachial, ulnar, and radial artery occlusion, as seen Immediately after surgery, the color of the fingers improved. Heparin at 500 unit/hour was infused intravenously after surgery. Hemodialysis resumed on the day after surgery, and no thrombus was found in intravascular spaces two days after surgery by duplex ultrasonography. The patient was discharged from hospital on the same day.

Discussion
Endovascular intervention and surgical intervention are recommended as treatments for the occlusion of vascular access [6,7]. On the other hand, none of the guidelines recommend or oppose massage as an immediate treatment for vascular access thrombosis. In clinical practice, a shunt massage is a procedure to break thrombi by external physical stimulation and disperse them to a central area [3]. The benefit of this procedure is that it can be performed immediately after a thrombotic occlusion occurs. At the same time, a risk associated with the procedure is that the dispersal of a coarse thrombus to a central site may lead to the development of a pulmonary embolism [8], whereas thrombi dispersing to the periphery represent a risk of brachial, ulnar, and radial artery occlusion, as seen

Discussion
Endovascular and surgical interventions are recommended as treatments for the occlusion of vascular accesses [6,7]. On the other hand, none of the guidelines recommend nor oppose massage as an immediate treatment for vascular access thrombosis. In clinical practice, a shunt massage is a procedure aimed to break thrombi by external physical stimulation and disperse them to a central area [3]. A strength of this procedure is that it can be performed immediately after a thrombotic occlusion is clinically evident. At the same time, a risk associated with the procedure is that the dispersion of a coarse thrombus may lead to the development of pulmonary embolism [8], whereas thrombi dispersing to the periphery represent a risk of brachial, ulnar and radial artery occlusion, as seen in the present case. Shunt massaging is a helpful technique that does not require any equipment. However, there are currently no studies nor reports that have quantitatively compared the benefits and risks of massages. Therefore, we believe that caution is mandatory. Although it was not performed in this case, we suggest performing ultrasonography, when possible, in order to determine beforehand the size and location of the thrombus.
The patient was diagnosed with AULI, which differs from common vascular access occlusions. Only 5% of acute limb ischemia occurs in the upper limb [9], and the primary cause is an atrial-fibrillation-based embolic event [10]. Additionally, there are some previous reports of AULI occurring after a shunt massage for acute thrombotic occlusions of vascular access, similar to this case [3,11]. The main therapies for acute limb ischemia are pharmacological thrombolysis using urokinase or a plasminogen activator, endovascular intervention using a thrombus aspiration catheter and finally surgical intervention using a Fogarty catheter [12]. Many historical case reports of AULI have used the same techniques [3,10].
In order to guarantee a full recovery, AULI requires treatment within a 6 h period [5]. If there is a prolonged ischemia, in 10-20% of cases an amputation is deemed necessary [13,14]. Patients with upper extremity artery occlusion can develop a compensatory collateral circulation through the interosseous arteries [15], and consequently are less likely to have complete ischemia than those with a lower extremity artery occlusion. However, collateral circulation was unable to develop in the present case considering the acute onset of occlusion. In addition, ischemia was likely to progress because the patient had severe arteriosclerosis due to long-term hemodialysis [16].
In case of AULI, it is important to evaluate progression risk of ischemia. The "five Ps" (pulseless, pallor, pain, paresthesia, and palsy) are used as clinical symptoms to diagnose ischemic lesions [17]. The patient met three of these criteria (pulseless, pallor, and pain), which suggested a clinical diagnosis of limb ischemia. Blood tests, duplex ultrasonography and CT angiography may aid the clinician [4]. In cases of advanced ischemia, a rapid transition from time-consuming examinations and conservative treatments to endovascular or surgical intervention is required; intraoperative angiography is also useful to reduce the procedural time.
In the present case, we performed surgical intervention promptly after diagnosis for two main reasons. Firstly, there was a large number of thrombi and a conservative approach such as pharmacological thrombolysis was unlikely to be resolutive, insoluble microthrombi may also have occluded the peripheral digital arteries [4]. Peripheral arteries, including digital arteries, are extremely narrow, which makes it difficult to reach thrombi using a catheter, and this situation could be fatal. Thus, surgical intervention was preferred to ensure reliable removal, since the thrombi were visible during the procedure. Secondly, thrombi were positioned in a complex manner in the brachial, radial and ulnar arteries, presenting with an overriding pattern. We anticipated that the removal of these thrombi would be difficult using a catheter alone, thus we performed an open insertion of a Fogarty catheter after an incision directly above the brachial artery , greatly improving reaching the thrombotic site. Consequently, almost all thrombi were removed. After surgery blood flow improved and hemodialysis could be resumed promptly, combining anticoagulant therapy.

Conclusions
We successfully treated a patient who developed brachial artery thrombosis after a massage for an AVG occlusion. Prompt treatment and thrombectomy are required for patients with AULI, and surgical intervention has been an effective procedure in this case. Institutional Review Board Statement: Ethical review and approval were waived for this study as per our Institutional Review Board, due to the nature of our research as a case report.
Informed Consent Statement: Informed consent was obtained from the subjects involved in the study to publish this paper.