Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients with Takayasu Arteritis and Renal Insufficiency

Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients with Takayasu Arteritis... Cardiovasc Intervent Radiol (2018) 41:998–1007 https://doi.org/10.1007/s00270-018-1936-x CLINICAL INVESTIGATION ARTERIAL INTERVENTIONS Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients with Takayasu Arteritis and Renal Insufficiency 1 1 1 1 • • • • Sujith Chacko George Joseph Viji Thomson Paul George 1 2 Oommen George Debashish Danda Received: 26 October 2017 / Accepted: 8 March 2018 / Published online: 16 March 2018 The Author(s) 2018 Abstract symptoms, better blood pressure control, improvement in Background Use of iodinated contrast agents for angiog- left ventricular systolic function and recovery or stabi- raphy in patients with renal insufficiency risks further lization of renal function. There were no early or late deterioration of renal function and its adverse sequelae. complications related to CO angiography. Three renal Objective To study the effectiveness and safety of carbon lesions that had restenosis at follow-up were managed dioxide (CO ) angiography in guiding percutaneous renal- successfully by repeat intervention. related interventions in patients with Takayasu arteritis and Conclusion CO angiography-guided renal-related inter- renal insufficiency. ventions are effective and safe in patients with Takayasu Methods Data on CO angiography-guided interventions arteritis and renal insufficiency; they significantly improve were obtained from a 23-year database of 692 Takayasu the care of such patients. arteritis patients who underwent percutaneous interventions and were analyzed retrospectively. Follow-up data were Keywords Renal insufficiency  Renal failure also obtained. The CO angiography system used was Takayasu arteritis  Carbon dioxide  Angioplasty developed in-house and was pressure-driven. Stent  Renal artery stenosis  Aortic stenosis Results Seven patients (6 female, age 16–59 years, base- Dissection  Pseudoaneurysm line serum creatinine 1.62–4.55 mg/dl, estimated glomerular filtration rate 12.2–36.9 ml/min/1.73 m ) underwent CO angiography-guided interventions: five underwent angioplasty or stenting to treat six stenotic/oc- cluded renal arteries, one underwent extensive endovas- Introduction cular repair for spontaneous focal abdominal aortic dissection with false lumen aneurysm and aorto-iliac true Carbon dioxide (CO ) has been used as an intra-arterial lumen narrowing, and one underwent balloon dilatation of contrast agent during angiography for more than four previously deployed aortic stents used to treat aortic decades [1]. Renal insufficiency is an important indication occlusion at two levels. Follow-up (median 5 years, range for the use of CO angiography, given the absence of 2 months–16 years) was obtained in all patients. All the nephrotoxicity with this agent [2]. Takayasu arteritis (TA), procedures were successful and resulted in relief of a chronic idiopathic granulomatous large vessel vasculitis affecting the aorta and its main branches [3], can produce renal insufficiency [4], mainly by causing renal artery & George Joseph stenosis [5]. At our center, prevalence of renal dysfunction joseph59@gmail.com in 118 patients with TA presenting during the period Department of Cardiology, Christian Medical College, 1963–1977 was 13.6% [6]. A recent study by Li et al. [4] Vellore 632004, India showed an overall prevalence of renal dysfunction of Department of Rheumatology, Christian Medical College, 11.4% in 411 patients with TA. There are no reports of the Vellore, India 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 999 use of CO angiography-guided interventions in TA apart CO to flow from the collection syringe to the patient. 2 2 from a single case report from our center in 2003 [7]; the Standard protocols were used for patient preparation and present study describes our 16-year single-center experi- digital subtraction angiography. Typically, the collection ence with CO angiography in guiding renal-related per- syringe volume was set at 20 ml for flush aortograms (to cutaneous interventions in patients with TA. deliver 60 ml of CO ) and 10 ml for selective angiograms (to deliver 30 ml of CO ). The quality of images obtained using this CO angiography system compared favorably Methods with that obtained with 50% iodixanol, a diluted alternative contrast agent, that is sometimes used in renal insufficiency Patients (Fig. 1B, C). Data on percutaneous interventions performed on patients with TA at our center (a large tertiary care referral hospital Results in South India) that were collected prospectively over 23 years and archived digitally were scrutinized. Cases Of 692 patients with TA who underwent percutaneous where CO angiography was utilized to guide percutaneous interventions to treat 1834 diseased arteries (including 425 interventions were selected, and the relevant case records renal arteries) over a 23-year period, seven patients and angiographic images were analyzed. Follow-up was (1.01%) underwent CO angiography-guided percutaneous obtained in all patients at 6- to 12-month intervals if stable, interventions because of renal insufficiency (Table 1). All but more frequently when indicated. Clinical status, seven patients (1 male/6 female, mean age 38 years) met imaging information and additional procedures done at both the American College of Rheumatology [8] and the follow-up were studied. All procedures were performed modified Ishikawa (clinical) criteria [9] for the diagnosis of after obtaining written informed consent. The institutional TA; all were hypertensive on multiple medications. All review board approved this retrospective study. For this patients were symptomatic at presentation, often with type of study formal consent is not required. recent worsening. Carbon dioxide Angiography System Renal Interventions The CO angiography system used (Fig. 1A) was devel- Five patients with significant renal artery stenosis under- oped in-house and has been operational for the last went CO angiography-guided renal angioplasty or stenting 17 years. It has no moving parts, and CO injection is using percutaneous femoral arterial access (Table 1, cases pressure-driven. Pressurized medical grade CO obtained 1–5; Fig. 2). In cases 1, 2 and 4, the renal artery was from a storage cylinder is passed through a Millipore filter engaged with a 7F renal-guiding catheter and the stenotic into a disposable 50 ml plastic collection syringe that is lesion was crossed with a 0.018-inch nitinol guidewire. In held firmly between fixed restraints on a metal platform. cases 3 and 5, the renal arteries were engaged with a 6F The piston of the collection syringe is variably restrained Judkins Right diagnostic catheter and a 0.035-inch angled by an assembly of swivelling blocks; the volume of the hydrophilic guidewire was used to cross the renal artery syringe is determined by the number of blocks in use in the lesion; this was replaced with a 0.035-inch stiff guidewire piston stopper assembly. A two-way stopcock attached to with 1-cm soft tip over which a long 7F femoral sheath was the collection syringe nozzle ensures that at no stage can advanced up to the renal artery ostium. Balloon-expandable the flow of CO bypass the syringe and go directly from bare metal stents were deployed in all the lesions except in cylinder to patient. Gas pressure in the collection syringe is case 5 where a stent had been deployed earlier. Balloon- kept at 4 kg/cm (nearly 4 atm) by appropriately adjusting dilatation pressures of 8 to 14 atm were used. A satisfac- the knob in the dual pressure gauge assembly which sep- tory result was obtained in all vessels without arately indicates cylinder (inflow) and tubing (outflow) complications. pressures. At this setting, the volume of CO delivered into the vessel is approximately three times the selected volume Aortic Interventions in the collection syringe; this can be verified by trial injection of CO into a collapsed plastic bag attached to the Two patients underwent CO angiography-guided aortic 2 2 three-way stopcock along the tubing. Prior to angiography, and ancillary interventions with successful outcomes and the tubing and angiographic catheter are flushed with CO without complications (Table 1, cases 6, 7; Fig. 3). to remove air and avoid explosive delivery of CO . For In case 6, extensive endovascular repair was performed CO injection, the two-way stopcock is turned 90 to allow for spontaneous focal abdominal aortic dissection with 123 1000 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Fig. 1 A Diagrammatic representation of the apparatus used for identical. B, C. Consecutive abdominal aortograms performed in carbon dioxide angiography. Every alternate block of the piston antero-posterior projection in a patient with renal failure using carbon stopper assembly has been left un-shaded to reveal the perpendicular dioxide and 50% iodixanol, respectively, with identical settings of rod around which the blocks can swivel 180; all the blocks are digital subtraction angiography false lumen aneurysm formation and aorto-iliac true lumen of the false lumen aneurysm, abolition of the aorto-iliac narrowing with 103 mmHg systolic pressure gradient. The pressure gradient and preserved flow into the left renal and celiac and left renal arteries were the only patent visceral celiac arteries. aortic branches. In the first sitting, aorto-iliac stenting was Case 7 had presented 7 months earlier with occlusions performed with a covered stent in the infra-renal aorta and of both renal arteries and of the aorta at two levels; the bare metal stents in both common iliac arteries. In a second aortic occlusions were recanalized and stented with bal- sitting 7 days later, a tapered aorto-uni-iliac endograft was loon-expandable stents, but the lesions were resistant to deployed in the abdominal aorta starting above the upper dilatation, and only partial opening was achieved with a limit of the aortic dissection (at the celiac artery ostium 9-mm-diameter non-compliant balloon. Renal function had level) and overlapping the earlier deployed stent below. subsequently deteriorated, and in the present sitting CO Flow into the left renal artery was preserved by con- angiography-guided balloon dilatation of both stents was structing a chimney graft. Flow into the celiac artery was performed using a 10-mm-diameter non-compliant balloon preserved using a bare metal stent deployed in chimney which resulted in further stent expansion and reduction in fashion. A satisfactory result was obtained with exclusion the aortic pressure gradient. This provided a sufficient 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1001 Table 1 Case and procedure details Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Baseline parameters Age (years)/Sex 59 F 45 M 30 F 28 F 38 F 50 F 16 F Takayasu arteritis diagnostic criteria met ACR criteria 5 of 6 5 of 6 5 of 6 3 of 6 5 of 6 3 of 6 4 of 6 Clinical 2 major, 4 minor 2 major, 3 minor 2 major, 4 minor 1 major, 2 minor 1 major, 3 minor 1 major, 4 minor 1 major, 5 minor criteria Limb blood pressure (mmHg) Upper 180/100 210/130 220/110 210/130 114/64 179/83 160/96 Lower 220/120 170/100 220/110 n/a 139/69 76/37 65 mean Number of anti-43 6 3 5 4 2 HTN drugs LV ejection 56 56 35 n/a 40 37 38 fraction (%) Creatinine (mg/ 3.27 3.50 1.62 1.80 4.55 3.39 1.90 dl) eGFR (ml/min/ 17.0 21.3 36.9 32.8 12.2 17.9 33.1 1.73 m ) Kidney size (cm) Right 9.0 Removed 9.8 11.8 9.7 7.0 8.8 Left 6.9 10.4 9.2 Removed Shrunken 8.6 Shrunken Renal artery status Right 70% proximal stenosis Absent (post-nephrectomy) Ostial occlusion 90% ostial stenosis 90% distal edge stenosis Occluded Occluded Left Occluded 90% stenosis proximally 80% ostial stenosis Absent (post- nephrectomy) Occluded Normal Occluded Abdominal Mildly ectatic aorta, Long infra-renal aortic Minor infra-renal Minor infra-renal narrowing Patent stent in infra- Focal dissection Aortic aorta status irregular in outline stenosis with 36 mmHg narrowing renal aorta with TL occlusions peak gradient narrowing and above the FL aneurysm; celiac and occluded SMA below the IMA renal arteries 1002 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Table 1 continued Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Presentation Uncontrolled HTN, Uncontrolled HTN, Acute pulmonary Uncontrolled HTN, pedal Recent pulmonary Abdominal pain, Dyspnea on blurring of vision, fatigue, pedal edema, edema, absent edema edema with bilateral lower exertion, worsening renal worsening renal function left upper limb accelerated HTN – limb bilateral lower function pulses, renal now controlled claudication limb bruit, HTN claudication Interventional procedures Carbon dioxide Right renal stenting Left renal stenting Bilateral renal Right renal stenting Balloon angioplasty of Aortic endograft, Dilatation of angiography- stenting right renal stent left aortic stents guided renal ? celiac procedures chimney stents, aorto- iliac stents Volume of Nil Nil Nil Nil Nil 4 ml Nil iodinated contrast used with above Earlier or later None Right nephrectomy 4 years Angioplasty for Left nephrectomy 14 years Both renal arteries, None Two-segment renal or aortic earlier. Infra-renal aortic bilateral renal earlier. Angioplasty for descending and aortic stenting procedures stenting 6 years later in-stent right renal in-stent abdominal aorta 7 months not requiring restenosis restenosis 3 and 6 years stented 1-16 years earlier. Right carbon 5 years later later earlier. Left renal renal auto- dioxide stent occluded. transplantation angiography 2 weeks later Follow-up status Duration of 15 months 13 years 5 years 12 years 2 months 12 months 16 years follow-up Limb blood pressure (mmHg) Upper 130/90 110/70 150/80 110/70 114/72 160/50 126/70 Lower n/a 96 systolic 150 systolic 120/80 140 systolic 170 systolic 136 systolic Number of anti-12 2 2 3 5 2 HTN drugs LV ejection n/a 55 69 56 n/a 49 58 fraction (%) Creatinine (mg/ 1.20 1.35 0.79 0.86 0.98 3.52 0.84 dl) eGFR (ml/min/ 39.5 55.1 75.7 72.5 56.4 17.2 75.0 1.73m2) S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1003 pressure head for the right kidney to be auto-transplanted 2 weeks later to the right iliac fossa with the right renal artery being anastomosed end-to-end to the right internal iliac artery. Outcome and Follow-Up CO angiography provided sufficiently clear visualization of the vascular anatomy and enabled achievement of suc- cessful outcomes in all the patients. Some patients felt mild transient abdominal discomfort immediately after CO injection, but none had nausea, vomiting, hypotension, narcosis or air contamination-related problems. There were no late complications related to CO angiography. All patients were followed-up after the CO angiography-gui- ded intervention (median duration 5 years, range 2 months to 16 years; Table 1). None of the patients had deteriora- tion in renal function or required dialysis; rather, renal function improved in 6 patients and stabilized in one. All patients experienced resolution of their symptoms. Blood pressure control improved, as also left ventricular systolic function that was initially depressed in some patients. Restenotic renal artery lesions seen at follow-up in cases 3 and 4 were treated by balloon dilatation; in case 3 this produced distal edge dissection in the right renal artery and required deployment of a stent. In case 7, progressive dilatation of the aortic stents was performed during sub- sequent follow-up visits. Comparison with Iodinated Contrast During the same period of time, 46 TA patients with ele- vated serum creatinine levels ([ 1.4 mg/dl) underwent interventions using iodinated contrast after intravenous hydration; of these, none with serum creatinine levels below 3.0 mg/dl developed sustained worsening of renal function or required dialysis, but one of two patients with serum creatinine C 3.0 mg/dl required long-term dialysis. On the other hand, none of the TA patients who underwent CO angiography-guided interventions, including four with serum creatinine C 3.0 mg/dl, had worsening of renal function or required dialysis. Discussion Contrast-induced nephropathy is one of the most common causes of hospital-acquired renal insufficiency and is associated with a mortality of 14%; pre-existing renal insufficiency poses the greatest risk for developing this condition [10]. Absence of nephrotoxicity is perhaps the biggest advantage CO provides as a contrast agent, though it has several other benefits including being non-allergic Table 1 continued Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Symptoms Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Angiographic/ Awaited Left renal and aortic stents Awaited after Normal right renal flow Awaited Patent stents Widely patent Doppler widely patent angioplasty for pattern with normal aortic stents findings bilateral flow pattern and transplant restenosis renal artery M male, F female, ACR American College of Rheumatology, HTN hypertension, LV left ventricle, n/a data not available, eGFR estimated glomerular filtration rate, ESR erythrocyte sedimentation rate, TL true lumen, FL false lumen, SMA superior mesenteric artery, IMA inferior mesenteric artery Some aspects of case 4 have been published earlier Ref. [7] Intra-arterial pressure *Angiographic appearance 1004 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Fig. 2 Carbon dioxide-guided renal artery interventions in patients angiogram (F) obtained 11 years later (5 years after interval infra- with Takayasu arteritis and renal insufficiency. All images are carbon renal aortic stenting) shows good long-term outcome. GtoI. Case 3. dioxide angiograms unless stated otherwise. Ato C. Case 1. Baseline Baseline angiogram (G) shows right renal artery occlusion (black angiogram (A) shows right renal artery stenosis (arrow). After stent arrow) and left renal artery stenosis (white arrow). Bilateral renal positioning (B) and deployment, the final angiogram (C) showed a artery stenting was performed (H) leading to normalization of renal good outcome. Dto F. Case 2. Baseline angiogram (D) shows ostial function. Conventional angiogram done 4 months later (I) shows left renal artery stenosis (arrow) and long infra-renal aorta narrowing. good short-term outcome Renal function normalized after left renal stenting (E). Conventional and inexpensive, having low viscosity, allowing use of digital subtraction angiography, stacking software, tilting unlimited total volumes and not being diluted by blood tables and reliable delivery systems, the quality of images [11]. With modern technology such as high-resolution obtained with CO angiography has improved considerably 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1005 123 1006 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… b Fig. 3 Carbon dioxide-guided aortic and ancillary interventions in showed that renal artery revascularization procedures were patients with Takayasu arteritis and renal insufficiency. Ato G. Case effective in salvaging renal function in children with TA- 6. Magnetic resonance angiograms in transverse (A) and coronal induced renal artery stenosis. However, an autopsy study (B) planes and carbon dioxide angiogram early (C) and late [15] on 25 TA patients showed that whereas non-specific, (D) frames in antero-posterior (AP) projection show a single (left) renal artery, focal abdominal aortic dissection, narrowing of the infra- ischemic and/or hypertensive glomerular changes were renal aorta and both common iliac arteries and a large false lumen present in 44% of kidney specimens, 56% showed specific aneurysm on the left lateral aspect of infra-renal aorta (black asterisk). glomerular pathologies, most commonly diffuse mesangial Carbon dioxide AP (E) and lateral (F) angiograms after infra-renal proliferative glomerulonephritis; extent of large arterial aortic and bilateral iliac artery stenting show relief of stenosis; the superior mesenteric and right renal arteries are not visualized. Carbon inflammatory infiltrates assessed by morphometric analysis dioxide AP angiogram (G) after deployment of a tapered endograft in was most in the latter condition suggesting a relationship the abdominal aorta and chimney grafts in the left renal and superior between the two phenomena. mesenteric arteries shows patency of these arteries; the false lumen This report highlights some characteristic features of aneurysm was no longer visualized in the late frames. Hto K. Case 7. Carbon dioxide AP angiogram (H) obtained 7 months after stenting percutaneous interventions in TA. Firstly, the high rate of of the lower thoracic-upper abdominal and infra-renal aorta (renal restenosis seen after bare metal renal artery stenting in TA. function had deteriorated since then) shows residual stenosis and non- Secondly, repeat intervention, mostly balloon angioplasty visualization of the renal arteries. The stents were further expanded alone, is usually successful in dealing with the problem of by balloon dilatation (I), and the right kidney was auto-transplanted (J) resulting is normalization of renal function. Conventional AP restenosis. Thirdly, stenotic lesions in TA may be very aortogram (K) obtained 11 years later shows widely patent aortic resistant to dilatation, but can be progressively opened up stents with serial balloon dilatations over multiple sittings. Lastly, spontaneous dissections and aneurysms seen in TA can be effectively treated by endovascular techniques with mini- [2]. In many cases, such as the ones presented in this report, mal morbidity. the entire percutaneous intervention can be performed without use of iodinated contrast. In case 6, a single angiogram using 4 ml of iodinated contrast diluted with Conclusion saline was used to confirm adequate collateral flow from the celiac artery to the superior and inferior mesenteric Renal-related percutaneous interventions can be effectively artery territories; this was done before deploying aortic and safely performed guided by CO angiography in endografts across the ostia of these already occluded ves- patients with TA and renal insufficiency. Such procedures sels because recanalization of these vessels would no result in relief of symptoms, better blood pressure control, longer be possible. An important prerequisite for successful improvement in left ventricular systolic function and CO angiography is gentle, controlled, non-explosive 2 recovery or stabilization of renal function. CO angiogra- delivery of the gas using a closed and ideally non-pres- phy is a useful adjunct to the interventional armamentarium surized system; this can be achieved by use a series of one- available to treat patients with TA and renal insufficiency. way valves with a flaccid reservoir or blood bag [11, 12]. Compliance with Ethical Standards The CO angiography system used in this study was a pressurized system, but with adequate attention to outflow Conflict of interest All the authors declare that they have no conflict pressure and syringe volume and by purging the system of interest. with CO gas before use, no significant problems have been encountered; the system has worked well in more than 100 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// patients over 17 years, is simple, inexpensive and easy to creativecommons.org/licenses/by/4.0/), which permits unrestricted use and has guided aorto-iliac, lower extremity, venous and use, distribution, and reproduction in any medium, provided you give complex endovascular procedures. appropriate credit to the original author(s) and the source, provide a Renal insufficiency is not uncommon in TA despite link to the Creative Commons license, and indicate if changes were made. these patients being young and having few co-morbidities [4, 6]. Renal insufficiency in TA is usually attributed to renal ischemia caused by vascular obstruction and renal References parenchymal damage induced by systemic hypertension; glomerular disease is considered exceptional [13]. Recent 1. Hawkins IF, Caridi JG. Carbon dioxide (CO ) digital subtraction clinical studies [5, 14] support this contention. Hong et al. angiography: 26 year experience at the University of Florida. Eur [5] found that 9.7% of TA patients with renal artery Radiol. 1998;8:391–402. involvement developed chronic renal insufficiency over a 90-month follow-up period. Similarly, Obiagwu et al. [14] 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1007 2. Hawkins IF, Cho KJ, Caridi JG. Carbon dioxide in angiography 9. Sharma BK, Jain S, Suri S, Numano F. Diagnostic criteria for to reduce the risk of contrast-induced nephropathy. Radiol Clin Takayasu arteritis. Int J Cardiol. 1996;54(Suppl):S141–7. North Am. 2009;47:813–25. 10. Nash K, Hafeez A, Hou S. Hospital-acquired renal insufficiency. 3. Kerr GS, Hallahan CW, Giordano J, Leavitt RY, Fauci AS, Am J Kidney Dis. 2002;39:930–6. Rottem M, Hoffman GS. Takayasu arteritis. Ann Intern Med. 11. Caridi JG, Cho KJ, Fauria C, Eghbalieh N. Carbon dioxide digital 1994;120:919–29. subtraction angiography (CO2 DSA): a comprehensive user guide 4. Li J, Li H, Sun F, Chen Z, Yang Y, Zhao J, Li M, Tian X, Zeng for all operators. Vascu Dis Manag. 2014;11(10):E221–56. X. Clinical characteristics of heart involvement in Chinese 12. Cherian MP, Mehta P, Gupta P, Kalyanpur TM, Jayesh SR, Rupa patients with Takayasu arteritis. J Rheumatol. 2017 Aug 15. R. Technical note: a simple and effective CO delivery system for https://doi.org/10.3899/jrheum.161514. Epub ahead of print. angiography using a blood bag. Indian J Radiol Imaging. 5. Hong S, Ghang B, Kim YG, Lee CK, Yoo B. Long-term out- 2009;19:203–5. comes of renal artery involvement in Takayasu arteritis. 13. Boubaker K, Kaaroud H, Goucha R, Kheder A. Renal injury in J Rheumatol. 2017;44:466–72. Takayasu’s arteritis. Nephrol Ther. 2014;10:451–6. 6. Alurkar VM, Cherian G, Sukumar IP, Krishnaswami S, Abraham 14. Obiagwu PN, Gajjar P, McCulloch M, Scott C, Numanoglu A, KA, Raju AR. Non-specific aortoarteritis—a clinical profile. Nourse P. Salvageability of renal function following renal Christian Medical College Alumni Journal. 1978; XII: 5–14. revascularisation in children with Takayasu’s arteritis-induced 7. Chandy ST, John B, Kamath P, John GT. Exclusive carbon renal artery stenosis. S Afr Med J. 2016;106:813–6. dioxide-guided renal artery stenting in a case of Takayasu’s 15. de Pablo P, Garcı´a-Torres R, Uribe N, Ramo´n G, Nava A, Sil- arteritis with a solitary functioning kidney. Indian Heart J. veira LH, Amezcua-Guerra LM, Martı´nez-Lavı´n M, Pineda C. 2003;55:272–4. Kidney involvement in Takayasu arteritis. Clin Exp Rheumatol. 8. Arend WP, et al. The American College of Rheumatology 1990 2007;25(1 Suppl 44):S10–4. criteria for the classification of Takayasu arteritis. Arthritis Rheum. 1990;33:1129–34. http://www.deepdyve.com/assets/images/DeepDyve-Logo-lg.png CardioVascular and Interventional Radiology Springer Journals

Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients with Takayasu Arteritis and Renal Insufficiency

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Abstract

Cardiovasc Intervent Radiol (2018) 41:998–1007 https://doi.org/10.1007/s00270-018-1936-x CLINICAL INVESTIGATION ARTERIAL INTERVENTIONS Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients with Takayasu Arteritis and Renal Insufficiency 1 1 1 1 • • • • Sujith Chacko George Joseph Viji Thomson Paul George 1 2 Oommen George Debashish Danda Received: 26 October 2017 / Accepted: 8 March 2018 / Published online: 16 March 2018 The Author(s) 2018 Abstract symptoms, better blood pressure control, improvement in Background Use of iodinated contrast agents for angiog- left ventricular systolic function and recovery or stabi- raphy in patients with renal insufficiency risks further lization of renal function. There were no early or late deterioration of renal function and its adverse sequelae. complications related to CO angiography. Three renal Objective To study the effectiveness and safety of carbon lesions that had restenosis at follow-up were managed dioxide (CO ) angiography in guiding percutaneous renal- successfully by repeat intervention. related interventions in patients with Takayasu arteritis and Conclusion CO angiography-guided renal-related inter- renal insufficiency. ventions are effective and safe in patients with Takayasu Methods Data on CO angiography-guided interventions arteritis and renal insufficiency; they significantly improve were obtained from a 23-year database of 692 Takayasu the care of such patients. arteritis patients who underwent percutaneous interventions and were analyzed retrospectively. Follow-up data were Keywords Renal insufficiency  Renal failure also obtained. The CO angiography system used was Takayasu arteritis  Carbon dioxide  Angioplasty developed in-house and was pressure-driven. Stent  Renal artery stenosis  Aortic stenosis Results Seven patients (6 female, age 16–59 years, base- Dissection  Pseudoaneurysm line serum creatinine 1.62–4.55 mg/dl, estimated glomerular filtration rate 12.2–36.9 ml/min/1.73 m ) underwent CO angiography-guided interventions: five underwent angioplasty or stenting to treat six stenotic/oc- cluded renal arteries, one underwent extensive endovas- Introduction cular repair for spontaneous focal abdominal aortic dissection with false lumen aneurysm and aorto-iliac true Carbon dioxide (CO ) has been used as an intra-arterial lumen narrowing, and one underwent balloon dilatation of contrast agent during angiography for more than four previously deployed aortic stents used to treat aortic decades [1]. Renal insufficiency is an important indication occlusion at two levels. Follow-up (median 5 years, range for the use of CO angiography, given the absence of 2 months–16 years) was obtained in all patients. All the nephrotoxicity with this agent [2]. Takayasu arteritis (TA), procedures were successful and resulted in relief of a chronic idiopathic granulomatous large vessel vasculitis affecting the aorta and its main branches [3], can produce renal insufficiency [4], mainly by causing renal artery & George Joseph stenosis [5]. At our center, prevalence of renal dysfunction joseph59@gmail.com in 118 patients with TA presenting during the period Department of Cardiology, Christian Medical College, 1963–1977 was 13.6% [6]. A recent study by Li et al. [4] Vellore 632004, India showed an overall prevalence of renal dysfunction of Department of Rheumatology, Christian Medical College, 11.4% in 411 patients with TA. There are no reports of the Vellore, India 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 999 use of CO angiography-guided interventions in TA apart CO to flow from the collection syringe to the patient. 2 2 from a single case report from our center in 2003 [7]; the Standard protocols were used for patient preparation and present study describes our 16-year single-center experi- digital subtraction angiography. Typically, the collection ence with CO angiography in guiding renal-related per- syringe volume was set at 20 ml for flush aortograms (to cutaneous interventions in patients with TA. deliver 60 ml of CO ) and 10 ml for selective angiograms (to deliver 30 ml of CO ). The quality of images obtained using this CO angiography system compared favorably Methods with that obtained with 50% iodixanol, a diluted alternative contrast agent, that is sometimes used in renal insufficiency Patients (Fig. 1B, C). Data on percutaneous interventions performed on patients with TA at our center (a large tertiary care referral hospital Results in South India) that were collected prospectively over 23 years and archived digitally were scrutinized. Cases Of 692 patients with TA who underwent percutaneous where CO angiography was utilized to guide percutaneous interventions to treat 1834 diseased arteries (including 425 interventions were selected, and the relevant case records renal arteries) over a 23-year period, seven patients and angiographic images were analyzed. Follow-up was (1.01%) underwent CO angiography-guided percutaneous obtained in all patients at 6- to 12-month intervals if stable, interventions because of renal insufficiency (Table 1). All but more frequently when indicated. Clinical status, seven patients (1 male/6 female, mean age 38 years) met imaging information and additional procedures done at both the American College of Rheumatology [8] and the follow-up were studied. All procedures were performed modified Ishikawa (clinical) criteria [9] for the diagnosis of after obtaining written informed consent. The institutional TA; all were hypertensive on multiple medications. All review board approved this retrospective study. For this patients were symptomatic at presentation, often with type of study formal consent is not required. recent worsening. Carbon dioxide Angiography System Renal Interventions The CO angiography system used (Fig. 1A) was devel- Five patients with significant renal artery stenosis under- oped in-house and has been operational for the last went CO angiography-guided renal angioplasty or stenting 17 years. It has no moving parts, and CO injection is using percutaneous femoral arterial access (Table 1, cases pressure-driven. Pressurized medical grade CO obtained 1–5; Fig. 2). In cases 1, 2 and 4, the renal artery was from a storage cylinder is passed through a Millipore filter engaged with a 7F renal-guiding catheter and the stenotic into a disposable 50 ml plastic collection syringe that is lesion was crossed with a 0.018-inch nitinol guidewire. In held firmly between fixed restraints on a metal platform. cases 3 and 5, the renal arteries were engaged with a 6F The piston of the collection syringe is variably restrained Judkins Right diagnostic catheter and a 0.035-inch angled by an assembly of swivelling blocks; the volume of the hydrophilic guidewire was used to cross the renal artery syringe is determined by the number of blocks in use in the lesion; this was replaced with a 0.035-inch stiff guidewire piston stopper assembly. A two-way stopcock attached to with 1-cm soft tip over which a long 7F femoral sheath was the collection syringe nozzle ensures that at no stage can advanced up to the renal artery ostium. Balloon-expandable the flow of CO bypass the syringe and go directly from bare metal stents were deployed in all the lesions except in cylinder to patient. Gas pressure in the collection syringe is case 5 where a stent had been deployed earlier. Balloon- kept at 4 kg/cm (nearly 4 atm) by appropriately adjusting dilatation pressures of 8 to 14 atm were used. A satisfac- the knob in the dual pressure gauge assembly which sep- tory result was obtained in all vessels without arately indicates cylinder (inflow) and tubing (outflow) complications. pressures. At this setting, the volume of CO delivered into the vessel is approximately three times the selected volume Aortic Interventions in the collection syringe; this can be verified by trial injection of CO into a collapsed plastic bag attached to the Two patients underwent CO angiography-guided aortic 2 2 three-way stopcock along the tubing. Prior to angiography, and ancillary interventions with successful outcomes and the tubing and angiographic catheter are flushed with CO without complications (Table 1, cases 6, 7; Fig. 3). to remove air and avoid explosive delivery of CO . For In case 6, extensive endovascular repair was performed CO injection, the two-way stopcock is turned 90 to allow for spontaneous focal abdominal aortic dissection with 123 1000 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Fig. 1 A Diagrammatic representation of the apparatus used for identical. B, C. Consecutive abdominal aortograms performed in carbon dioxide angiography. Every alternate block of the piston antero-posterior projection in a patient with renal failure using carbon stopper assembly has been left un-shaded to reveal the perpendicular dioxide and 50% iodixanol, respectively, with identical settings of rod around which the blocks can swivel 180; all the blocks are digital subtraction angiography false lumen aneurysm formation and aorto-iliac true lumen of the false lumen aneurysm, abolition of the aorto-iliac narrowing with 103 mmHg systolic pressure gradient. The pressure gradient and preserved flow into the left renal and celiac and left renal arteries were the only patent visceral celiac arteries. aortic branches. In the first sitting, aorto-iliac stenting was Case 7 had presented 7 months earlier with occlusions performed with a covered stent in the infra-renal aorta and of both renal arteries and of the aorta at two levels; the bare metal stents in both common iliac arteries. In a second aortic occlusions were recanalized and stented with bal- sitting 7 days later, a tapered aorto-uni-iliac endograft was loon-expandable stents, but the lesions were resistant to deployed in the abdominal aorta starting above the upper dilatation, and only partial opening was achieved with a limit of the aortic dissection (at the celiac artery ostium 9-mm-diameter non-compliant balloon. Renal function had level) and overlapping the earlier deployed stent below. subsequently deteriorated, and in the present sitting CO Flow into the left renal artery was preserved by con- angiography-guided balloon dilatation of both stents was structing a chimney graft. Flow into the celiac artery was performed using a 10-mm-diameter non-compliant balloon preserved using a bare metal stent deployed in chimney which resulted in further stent expansion and reduction in fashion. A satisfactory result was obtained with exclusion the aortic pressure gradient. This provided a sufficient 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1001 Table 1 Case and procedure details Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Baseline parameters Age (years)/Sex 59 F 45 M 30 F 28 F 38 F 50 F 16 F Takayasu arteritis diagnostic criteria met ACR criteria 5 of 6 5 of 6 5 of 6 3 of 6 5 of 6 3 of 6 4 of 6 Clinical 2 major, 4 minor 2 major, 3 minor 2 major, 4 minor 1 major, 2 minor 1 major, 3 minor 1 major, 4 minor 1 major, 5 minor criteria Limb blood pressure (mmHg) Upper 180/100 210/130 220/110 210/130 114/64 179/83 160/96 Lower 220/120 170/100 220/110 n/a 139/69 76/37 65 mean Number of anti-43 6 3 5 4 2 HTN drugs LV ejection 56 56 35 n/a 40 37 38 fraction (%) Creatinine (mg/ 3.27 3.50 1.62 1.80 4.55 3.39 1.90 dl) eGFR (ml/min/ 17.0 21.3 36.9 32.8 12.2 17.9 33.1 1.73 m ) Kidney size (cm) Right 9.0 Removed 9.8 11.8 9.7 7.0 8.8 Left 6.9 10.4 9.2 Removed Shrunken 8.6 Shrunken Renal artery status Right 70% proximal stenosis Absent (post-nephrectomy) Ostial occlusion 90% ostial stenosis 90% distal edge stenosis Occluded Occluded Left Occluded 90% stenosis proximally 80% ostial stenosis Absent (post- nephrectomy) Occluded Normal Occluded Abdominal Mildly ectatic aorta, Long infra-renal aortic Minor infra-renal Minor infra-renal narrowing Patent stent in infra- Focal dissection Aortic aorta status irregular in outline stenosis with 36 mmHg narrowing renal aorta with TL occlusions peak gradient narrowing and above the FL aneurysm; celiac and occluded SMA below the IMA renal arteries 1002 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Table 1 continued Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Presentation Uncontrolled HTN, Uncontrolled HTN, Acute pulmonary Uncontrolled HTN, pedal Recent pulmonary Abdominal pain, Dyspnea on blurring of vision, fatigue, pedal edema, edema, absent edema edema with bilateral lower exertion, worsening renal worsening renal function left upper limb accelerated HTN – limb bilateral lower function pulses, renal now controlled claudication limb bruit, HTN claudication Interventional procedures Carbon dioxide Right renal stenting Left renal stenting Bilateral renal Right renal stenting Balloon angioplasty of Aortic endograft, Dilatation of angiography- stenting right renal stent left aortic stents guided renal ? celiac procedures chimney stents, aorto- iliac stents Volume of Nil Nil Nil Nil Nil 4 ml Nil iodinated contrast used with above Earlier or later None Right nephrectomy 4 years Angioplasty for Left nephrectomy 14 years Both renal arteries, None Two-segment renal or aortic earlier. Infra-renal aortic bilateral renal earlier. Angioplasty for descending and aortic stenting procedures stenting 6 years later in-stent right renal in-stent abdominal aorta 7 months not requiring restenosis restenosis 3 and 6 years stented 1-16 years earlier. Right carbon 5 years later later earlier. Left renal renal auto- dioxide stent occluded. transplantation angiography 2 weeks later Follow-up status Duration of 15 months 13 years 5 years 12 years 2 months 12 months 16 years follow-up Limb blood pressure (mmHg) Upper 130/90 110/70 150/80 110/70 114/72 160/50 126/70 Lower n/a 96 systolic 150 systolic 120/80 140 systolic 170 systolic 136 systolic Number of anti-12 2 2 3 5 2 HTN drugs LV ejection n/a 55 69 56 n/a 49 58 fraction (%) Creatinine (mg/ 1.20 1.35 0.79 0.86 0.98 3.52 0.84 dl) eGFR (ml/min/ 39.5 55.1 75.7 72.5 56.4 17.2 75.0 1.73m2) S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1003 pressure head for the right kidney to be auto-transplanted 2 weeks later to the right iliac fossa with the right renal artery being anastomosed end-to-end to the right internal iliac artery. Outcome and Follow-Up CO angiography provided sufficiently clear visualization of the vascular anatomy and enabled achievement of suc- cessful outcomes in all the patients. Some patients felt mild transient abdominal discomfort immediately after CO injection, but none had nausea, vomiting, hypotension, narcosis or air contamination-related problems. There were no late complications related to CO angiography. All patients were followed-up after the CO angiography-gui- ded intervention (median duration 5 years, range 2 months to 16 years; Table 1). None of the patients had deteriora- tion in renal function or required dialysis; rather, renal function improved in 6 patients and stabilized in one. All patients experienced resolution of their symptoms. Blood pressure control improved, as also left ventricular systolic function that was initially depressed in some patients. Restenotic renal artery lesions seen at follow-up in cases 3 and 4 were treated by balloon dilatation; in case 3 this produced distal edge dissection in the right renal artery and required deployment of a stent. In case 7, progressive dilatation of the aortic stents was performed during sub- sequent follow-up visits. Comparison with Iodinated Contrast During the same period of time, 46 TA patients with ele- vated serum creatinine levels ([ 1.4 mg/dl) underwent interventions using iodinated contrast after intravenous hydration; of these, none with serum creatinine levels below 3.0 mg/dl developed sustained worsening of renal function or required dialysis, but one of two patients with serum creatinine C 3.0 mg/dl required long-term dialysis. On the other hand, none of the TA patients who underwent CO angiography-guided interventions, including four with serum creatinine C 3.0 mg/dl, had worsening of renal function or required dialysis. Discussion Contrast-induced nephropathy is one of the most common causes of hospital-acquired renal insufficiency and is associated with a mortality of 14%; pre-existing renal insufficiency poses the greatest risk for developing this condition [10]. Absence of nephrotoxicity is perhaps the biggest advantage CO provides as a contrast agent, though it has several other benefits including being non-allergic Table 1 continued Feature Case 1 Case 2 Case 3 Case 4 Case 5 Case 6 Case 7 Symptoms Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Asymptomatic Angiographic/ Awaited Left renal and aortic stents Awaited after Normal right renal flow Awaited Patent stents Widely patent Doppler widely patent angioplasty for pattern with normal aortic stents findings bilateral flow pattern and transplant restenosis renal artery M male, F female, ACR American College of Rheumatology, HTN hypertension, LV left ventricle, n/a data not available, eGFR estimated glomerular filtration rate, ESR erythrocyte sedimentation rate, TL true lumen, FL false lumen, SMA superior mesenteric artery, IMA inferior mesenteric artery Some aspects of case 4 have been published earlier Ref. [7] Intra-arterial pressure *Angiographic appearance 1004 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… Fig. 2 Carbon dioxide-guided renal artery interventions in patients angiogram (F) obtained 11 years later (5 years after interval infra- with Takayasu arteritis and renal insufficiency. All images are carbon renal aortic stenting) shows good long-term outcome. GtoI. Case 3. dioxide angiograms unless stated otherwise. Ato C. Case 1. Baseline Baseline angiogram (G) shows right renal artery occlusion (black angiogram (A) shows right renal artery stenosis (arrow). After stent arrow) and left renal artery stenosis (white arrow). Bilateral renal positioning (B) and deployment, the final angiogram (C) showed a artery stenting was performed (H) leading to normalization of renal good outcome. Dto F. Case 2. Baseline angiogram (D) shows ostial function. Conventional angiogram done 4 months later (I) shows left renal artery stenosis (arrow) and long infra-renal aorta narrowing. good short-term outcome Renal function normalized after left renal stenting (E). Conventional and inexpensive, having low viscosity, allowing use of digital subtraction angiography, stacking software, tilting unlimited total volumes and not being diluted by blood tables and reliable delivery systems, the quality of images [11]. With modern technology such as high-resolution obtained with CO angiography has improved considerably 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1005 123 1006 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… b Fig. 3 Carbon dioxide-guided aortic and ancillary interventions in showed that renal artery revascularization procedures were patients with Takayasu arteritis and renal insufficiency. Ato G. Case effective in salvaging renal function in children with TA- 6. Magnetic resonance angiograms in transverse (A) and coronal induced renal artery stenosis. However, an autopsy study (B) planes and carbon dioxide angiogram early (C) and late [15] on 25 TA patients showed that whereas non-specific, (D) frames in antero-posterior (AP) projection show a single (left) renal artery, focal abdominal aortic dissection, narrowing of the infra- ischemic and/or hypertensive glomerular changes were renal aorta and both common iliac arteries and a large false lumen present in 44% of kidney specimens, 56% showed specific aneurysm on the left lateral aspect of infra-renal aorta (black asterisk). glomerular pathologies, most commonly diffuse mesangial Carbon dioxide AP (E) and lateral (F) angiograms after infra-renal proliferative glomerulonephritis; extent of large arterial aortic and bilateral iliac artery stenting show relief of stenosis; the superior mesenteric and right renal arteries are not visualized. Carbon inflammatory infiltrates assessed by morphometric analysis dioxide AP angiogram (G) after deployment of a tapered endograft in was most in the latter condition suggesting a relationship the abdominal aorta and chimney grafts in the left renal and superior between the two phenomena. mesenteric arteries shows patency of these arteries; the false lumen This report highlights some characteristic features of aneurysm was no longer visualized in the late frames. Hto K. Case 7. Carbon dioxide AP angiogram (H) obtained 7 months after stenting percutaneous interventions in TA. Firstly, the high rate of of the lower thoracic-upper abdominal and infra-renal aorta (renal restenosis seen after bare metal renal artery stenting in TA. function had deteriorated since then) shows residual stenosis and non- Secondly, repeat intervention, mostly balloon angioplasty visualization of the renal arteries. The stents were further expanded alone, is usually successful in dealing with the problem of by balloon dilatation (I), and the right kidney was auto-transplanted (J) resulting is normalization of renal function. Conventional AP restenosis. Thirdly, stenotic lesions in TA may be very aortogram (K) obtained 11 years later shows widely patent aortic resistant to dilatation, but can be progressively opened up stents with serial balloon dilatations over multiple sittings. Lastly, spontaneous dissections and aneurysms seen in TA can be effectively treated by endovascular techniques with mini- [2]. In many cases, such as the ones presented in this report, mal morbidity. the entire percutaneous intervention can be performed without use of iodinated contrast. In case 6, a single angiogram using 4 ml of iodinated contrast diluted with Conclusion saline was used to confirm adequate collateral flow from the celiac artery to the superior and inferior mesenteric Renal-related percutaneous interventions can be effectively artery territories; this was done before deploying aortic and safely performed guided by CO angiography in endografts across the ostia of these already occluded ves- patients with TA and renal insufficiency. Such procedures sels because recanalization of these vessels would no result in relief of symptoms, better blood pressure control, longer be possible. An important prerequisite for successful improvement in left ventricular systolic function and CO angiography is gentle, controlled, non-explosive 2 recovery or stabilization of renal function. CO angiogra- delivery of the gas using a closed and ideally non-pres- phy is a useful adjunct to the interventional armamentarium surized system; this can be achieved by use a series of one- available to treat patients with TA and renal insufficiency. way valves with a flaccid reservoir or blood bag [11, 12]. Compliance with Ethical Standards The CO angiography system used in this study was a pressurized system, but with adequate attention to outflow Conflict of interest All the authors declare that they have no conflict pressure and syringe volume and by purging the system of interest. with CO gas before use, no significant problems have been encountered; the system has worked well in more than 100 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http:// patients over 17 years, is simple, inexpensive and easy to creativecommons.org/licenses/by/4.0/), which permits unrestricted use and has guided aorto-iliac, lower extremity, venous and use, distribution, and reproduction in any medium, provided you give complex endovascular procedures. appropriate credit to the original author(s) and the source, provide a Renal insufficiency is not uncommon in TA despite link to the Creative Commons license, and indicate if changes were made. these patients being young and having few co-morbidities [4, 6]. Renal insufficiency in TA is usually attributed to renal ischemia caused by vascular obstruction and renal References parenchymal damage induced by systemic hypertension; glomerular disease is considered exceptional [13]. Recent 1. Hawkins IF, Caridi JG. Carbon dioxide (CO ) digital subtraction clinical studies [5, 14] support this contention. Hong et al. angiography: 26 year experience at the University of Florida. Eur [5] found that 9.7% of TA patients with renal artery Radiol. 1998;8:391–402. involvement developed chronic renal insufficiency over a 90-month follow-up period. Similarly, Obiagwu et al. [14] 123 S. Chacko et al.: Carbon dioxide Angiography-Guided Renal-Related Interventions in Patients… 1007 2. Hawkins IF, Cho KJ, Caridi JG. Carbon dioxide in angiography 9. Sharma BK, Jain S, Suri S, Numano F. Diagnostic criteria for to reduce the risk of contrast-induced nephropathy. Radiol Clin Takayasu arteritis. Int J Cardiol. 1996;54(Suppl):S141–7. North Am. 2009;47:813–25. 10. Nash K, Hafeez A, Hou S. Hospital-acquired renal insufficiency. 3. Kerr GS, Hallahan CW, Giordano J, Leavitt RY, Fauci AS, Am J Kidney Dis. 2002;39:930–6. Rottem M, Hoffman GS. Takayasu arteritis. Ann Intern Med. 11. Caridi JG, Cho KJ, Fauria C, Eghbalieh N. Carbon dioxide digital 1994;120:919–29. subtraction angiography (CO2 DSA): a comprehensive user guide 4. Li J, Li H, Sun F, Chen Z, Yang Y, Zhao J, Li M, Tian X, Zeng for all operators. Vascu Dis Manag. 2014;11(10):E221–56. X. Clinical characteristics of heart involvement in Chinese 12. Cherian MP, Mehta P, Gupta P, Kalyanpur TM, Jayesh SR, Rupa patients with Takayasu arteritis. J Rheumatol. 2017 Aug 15. R. Technical note: a simple and effective CO delivery system for https://doi.org/10.3899/jrheum.161514. Epub ahead of print. angiography using a blood bag. Indian J Radiol Imaging. 5. Hong S, Ghang B, Kim YG, Lee CK, Yoo B. Long-term out- 2009;19:203–5. comes of renal artery involvement in Takayasu arteritis. 13. Boubaker K, Kaaroud H, Goucha R, Kheder A. Renal injury in J Rheumatol. 2017;44:466–72. Takayasu’s arteritis. Nephrol Ther. 2014;10:451–6. 6. Alurkar VM, Cherian G, Sukumar IP, Krishnaswami S, Abraham 14. Obiagwu PN, Gajjar P, McCulloch M, Scott C, Numanoglu A, KA, Raju AR. Non-specific aortoarteritis—a clinical profile. Nourse P. Salvageability of renal function following renal Christian Medical College Alumni Journal. 1978; XII: 5–14. revascularisation in children with Takayasu’s arteritis-induced 7. Chandy ST, John B, Kamath P, John GT. Exclusive carbon renal artery stenosis. S Afr Med J. 2016;106:813–6. dioxide-guided renal artery stenting in a case of Takayasu’s 15. de Pablo P, Garcı´a-Torres R, Uribe N, Ramo´n G, Nava A, Sil- arteritis with a solitary functioning kidney. Indian Heart J. veira LH, Amezcua-Guerra LM, Martı´nez-Lavı´n M, Pineda C. 2003;55:272–4. Kidney involvement in Takayasu arteritis. Clin Exp Rheumatol. 8. Arend WP, et al. 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CardioVascular and Interventional RadiologySpringer Journals

Published: Mar 16, 2018

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