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Available online at www.sciencedirect.com
www.elsevier.com/locate/semvascsurg
Renal fibromuscular dysplasia Albeir Y. Mousan, and Gurpreet Gill Department of Surgery, R. C. Byrd Health Sciences Center, West Virginia University, 3110 MacCorkle Avenue SE, Charleston, WV 25304
article info
abstra ct Renal artery fibromuscular dysplasia is a noninflammatory, nonatherosclerotic vasculopathy that can affect renal arteries at various degrees with different severity. The etiology is still unknown, but there is a strong belief that a genetic disorder is the main cause for the pathogenesis of this disease. The main presentation is a sudden onset of recalcitrant hypertension at a young age, which is usually resistant to medical treatment. Once renal artery fibromuscular dysplasia is suspected, several diagnostic tools are available to make an accurate diagnosis. The advent of minimally invasive interventions has revolutionized the options for treatment. This update should provide the clinician with a base understanding of available evidence for diagnosing and treating renal artery fibromuscular dysplasia. & 2014 Elsevier Inc. All rights reserved.
1.
Introduction
Fibromuscular dysplasia (FMD) is a nonatherosclerotic, noninflammatory arterial wall disease that typically affects small- to medium-sized vessels. Despite many theories, the etiology of renal artery fibromuscular dysplasia (RAFMD) remains unknown (Fig 1). All respected authorities agree that a genetic component plays an important role in this disease because it mostly affects Caucasians. In addition, an association between RAFMD and the HLA-DRw6 histocompatibility antigen has also been described [1,2]. FMD occurs predominately in middle-aged females, but it can also affect male patients at different age spectrums. The most common nonatherosclerotic disease related to renovascular hypertension is RAFMD, which accounts for o10% of patients with symptomatic renal artery stenosis. FMD is not exclusive to the renal arteries, it can also affect the extracranial carotid arteries at the same frequency [3], the external iliac arteries (Fig 2) [4,5], and even mesenteric arterial involvement has been reported [6,7]. Coronary vessel involvement with FMD can also occur and can predispose to dissection [8].
n
Corresponding author. E-mail address: [email protected] (A.Y. Mousa).
http://dx.doi.org/10.1053/j.semvascsurg.2014.06.006 0895-7967/$ - see front matter & 2014 Elsevier Inc. All rights reserved.
There are three main pathologic appearances for RAFMD; medial dysplasia is the most common type, accounting for almost 80% of cases. The most characteristic angiographic appearance for the medial type is the “string of beads” appearance [9], as demonstrated in Figure 1. The other two types of RAFMD are intimal fibroplasia and adventitial fibroplasia. The right main renal artery is more commonly affected by RAFMD, but bilateral vessel involvement can occur in up to 35% of patients [10]. Anatomical outcomes of RAFMD include stenosis, occlusion, or aneurysmal formation. The main physiologic concern in patients with RAFMD is uncontrolled hypertension; however, unlike atherosclerotic renal artery disease, RAFMD is rarely associated with loss of renal function, although loss of renal mass can occur in up to 63% of patients [11,12]. Progression of stenosis can occur in up to 37% of patients [12], yet renal artery occlusion with subsequent parenchymal infarct is rare [13,14]. The nature of the disease progression, along with minimal effects on renal function, have encouraged some vascular specialists to recommend medical treatment only as the initial therapy for patients with RAFMD.
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Fig. 1 – Renal artery angiogram showing typical angiographic “string of beads” appearance of fibromuscular dysplasia. Although questioned recently, patients with recalcitrant hypertension may benefit from renal artery angioplasty and stenting, and endovascular treatment with angioplasty has been widely accepted as the standard of care. We previously reported our extensive experience with renal artery stenting for atherosclerotic lesions [15,16].
2.
Clinical presentation
Most patients with RAFMD are asymptomatic, but the most common presentation in symptomatic patients is severe hypertension. These presentations are directly related to the underlying pathology (ie, stenosis, occlusion, or aneurysm formation). All available epidemiologic studies have confirmed that a hemodynamically significant stenotic lesion of the renal artery is the most common cause of secondary hypertension [17–19]. Nevertheless, the incidence of
Fig. 2 – External iliac artery angiogram showing fibromuscular dysplasia appearance.
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renovascular hypertension in the general population is estimated to be 1% to 3% [20,21]. Out of that population, FMD can affect up to 0.5%, therefore, it is considered the most common cause for secondary hypertension in children and young adults [11,12]. The most common population is women between their 3rd and 6th decades. The prevalence of FMD in the general population is still not well characterized, but there is growing evidence that the prevalence is higher than previously thought. In one study, patients with RAFMD constituted 3.8% of 1,862 patients who had renal artery angiograms [22]. Mean age for diagnosing RAFMD is the 6th decade, and this older age indicates that the disease is still underestimated, however, it can occur in any age group [23– 25]. We recommend that any patient with recalcitrant hypertension with triple antihypertensive therapy, including one diuretic, should be considered for a workup for RAFMD. It is worth mentioning that both main pathologies for renal artery stenosis (ie, atherosclerosis and FMD) can produce similar hemodynamic effects with potential sequelae of recalcitrant hypertension and deterioration of renal function. For a better understanding, we rely significantly on Goldblatt’s model, that is, one-kidney, one clip versus two kidneys, and one clip regarding renovascular hypertension and underlying volume versus sodium changes [26]. The clinical presentation of RAFMD is usually acute onset of recalcitrant hypertension in young patients, predominately in female patients. Because RAFMD is a potentially curable source of hypertension, early diagnosis is imperative to initiate adequate therapy. Unexplained malignant hypertension, especially in young females, should alert clinicians to rule out secondary causes, including RAFMD [27]. Kim et al [28] analyzed a very interesting recent registry of 615 patients with FMD. In that registry, the mean age at diagnosis was 51.9 years. Hypertension and headache were the most prevalent presenting symptoms in that study, with no sex predilection; in the mean time, both hypertension and headache were the most common presenting symptoms, leading to the diagnosis of RAFMD for both sexes. Notably, females were more likely to present with extracranial carotid/ vertebral artery stenosis than men, with a higher chance of pulsatile tinnitus (35% v 9%; P ¼ .0002). In that study, men were more likely to present with signs or symptoms of renal artery involvement, such as flank or abdominal pain, azotemia, and renal infarction (42% v 4%; P ¼ .006). In the entire cohort, renal and extracranial vessel involvements were more common than other arterial involvement (7% and 72%). Men were more likely to have RAFMD than carotid involvement (90% v 74%), and women were more likely to present with extracranial carotid disease (74% v 44%). Generally, dissection/aneurysms were common among patients in that registry with 22% of patients having one or more arterial dissections and 21% of patients having one or more aneurysms. Men were more likely to present with aneurysms than dissections (41% v 20%), and females were more likely to present with dissections (39% v 20%; P ¼ .002). Dissections were more likely to occur at extracranial carotid arteries (16%), followed by vertebral arteries (4.2%) and renal arteries (4%). Although men constituted a minority of 8% in that registry, the main presentations for males were still arterial aneurysms or dissections. Females were more likely to
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present with clinical manifestation related to the extracranial carotid artery.
2.1.
Diagnosis
Diagnosis of RAFMD is predominantly dependent on angiographic characteristics of lesions, as arterial tissue samples are rarely available. In a contemporary practice, objective evaluation of patients with renovascular hypertension should begin with a renal artery duplex ultrasound that may show signs of renal artery stenosis in the form of an elevated peak systolic velocity and an aliasing effect, along with a size difference between the two kidneys and a possible elevated reno-aortic ratio Z3.5. Details of renal duplex ultrasound is illustrated at different chapter of that edition. The utility of duplex ultrasound (DUS) in patients with RAFMD has been evaluated in a few studies. Olin et al [29] reported an overall sensitivity of DUS compared with arteriography of 0.98, a specificity of 0.98, a positive predictive value of 0.99, and a negative predictive value of 0.97. The authors concluded that DUS scanning of the renal arteries is an ideal initial screening test, as it is noninvasive and correlates accurately with the degree of renal artery stenosis [29]. However, DUS is an operator-dependent test and can be technically challenging when it comes to evaluating the mid to distal arterial segment. Turbulence, a noisy velocity shift along the arterial segment or beadings on the longitudinal image, can raise suspicion for RAFMD. The diagnosis can be confirmed by a multidetector computed tomography (CT) scan [15] and magnetic resonance angiography [16]. CT angiography plays an important role as well. A recent report from the Mayo Clinic evaluated the incidence, demographics, and clinical presentation of patients diagnosed with RAFMD during a 12-year period using the living donor renal protocol. Of 2,640 patients, 68 were diagnosed with RAFMD (2.6%, 59 were female). The mean age was 52 years and it occurred bilaterally in 32% of patients [30]. An interesting recent retrospective cross-sectional study evaluated the clinical relevance of a binary angiographic classification of RAFMD lesions, either unifocal or multifocal (Z2 focal stenosis), based on CT angiography or magnetic resonance angiography. The interesting conclusion of that study is that the phenotype of the lesion determined the clinical outcomes. Of 337 patients, 82% were multifocal and that group was older (median age of 49 v 30 years), they presented with hypertension at an older age, it was more dominant in females, and fewer had bilateral disease (38% v 79%) [31]. Magnetic resonance angiography and computed tomography angiography are still limited and cannot accurately diagnose any segmental or subsegmental vessel disease. In addition, magnetic resonance angiography might also be limited by motion artifact and can overestimate lesions. To date, subtraction angiography with intravascular ultrasound (IVUS) is the most accurate method for diagnosing RAFMD, demonstrating a classic “string of beads” appearance for the medial type or focal narrowing for the intimal type of RAFMD [32]. We believe that the single most important advancement that has occurred in the world of diagnostic renal tools is the
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development of IVUS (Fig 3). Adding IVUS to renal angiography will minimize the inherited limitations of angiography regarding the hemodynamic effects of the lesions. Also, the use of pressure gradients is controversial because the webs associated with FMD can be “compressed” with a catheter or “pressure wire,” and this may cause a false-negative reading. Additionally, there could be a flow-mediated impact on downstream tissue that is independent of the gradient. However, IVUS gives an accurate understanding of the severity of the stenosis and assists in accurate sizing of balloons. Also, utilizing IVUS to evaluate restenosis after endovascular therapy for RAFMD can be extremely valuable.
2.2.
Fate
RAFMD can cause nonatheromatous arterial stenosis with webs or segmental arterial constrictions that may contribute to parenchymal infarction as an initial presentation [33]. Dissection has been reported as a possible presentation of or outcome for patients with RAFMD [34]. Renal artery aneurysms may occur and the recommended treatment is a covered stent or open surgical repair [35,36].
2.3.
Treatments
When intervention is indicated for patients with recalcitrant hypertension, renal artery angioplasty with or without stenting is currently the most widely recommended initial treatment. Many authors, including our group, have reported on their long-term experience with renal artery stenting for atherosclerotic lesions [17–19]. When it comes to RAFMD, only a handful of studies have analyzed the long-term outcomes after endovascular interventions for symptomatic patients [3,10,37]. Although there is no recommended surgical treatment for asymptomatic RAFMD, these patients should be given antiplatelets and statin therapy, if not contraindicated [25]. The appropriate treatment should be offered to all patients with symptomatic RAFMD [1,38].
Fig. 3 – Intravascular ultrasound (IVUS) demonstration of intravascular appearance of fibromuscular dysplasia— web-like projection—including chromo IVUS [4]. (Color version of figure is available online.)
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Endovascular therapy
Balloon angioplasty has been shown to be successful by disrupting the “webs" of tissue in the renal artery [39]. Percutaneous intervention for symptomatic RAFMD has replaced surgical therapy as the first line of treatment [10]. In our recent publication [37], we evaluated the short- and long-term outcomes of percutaneous transluminal intervention in patients with symptomatic renal artery stenosis due to RAFMD and/or the combination of RAFMD with aorto-ostial atherosclerotic disease. A retrospective analysis was conducted for all patients with RAFMD who underwent transcatheter therapy during a 10-year period. Blood pressure (BP) measurement, the number of BP medications, and hypertension as defined by systolic BP >140 mm Hg and/or diastolic BP >90 mm Hg were recorded. Renal function was defined by an estimated glomerular filtration rate (eGFR). Restenosis was defined by stenosis >60% as determined by renal artery duplex and/or angiography. Freedom from events (ie, restenosis, renal failure, or recurrent hypertension) was performed using a life-table analysis. We examined 43 procedures in 35 patients with RAFMD. Thirty-two patients (91%) were women, with a mean age of 61.9 years. The technical success rate was 100%, with adjunctive stent placement required in the FMD segment for dissection in one patient (2.3%) and in the nonFMD aorto-ostial atherosclerotic lesion in four patients (9.3%). Short-term outcomes were the following: the majority (69%) had an immediate clinical benefit for hypertension, 63% improved with less than or equal to preoperative BP medications, and 6% were cured without BP medications. Postintervention, 17% remained at a moderately reduced renal function (o60 mL/min), and the percentage >60 mL/min eGFR increased significantly (from 51% to 69%; P ¼ .002). For the entire cohort, renal function (mean eGFR) increased significantly from 71.9 mL/min þ 5.8 to 80.8 mL/min þ 5.2; P ¼ .007). Long-term outcomes were the following: freedom from recurrent or worsening hypertension (>140 mm Hg systolic BP and >90 mm Hg diastolic BP) was 93%, 75%, and 41%; and freedom from reduced renal function (eGFR o30 mL/minute) was 100%, 95%, and 64% at 1, 5, and 8 years, respectively. Patients with reduced baseline renal function (o60 mL/min) and combined atherosclerotic disease were more likely to experience long-term reduced renal function (eGFR o30 mL/min; P ¼ .003). The primary and assisted primary patency rates were 95%, 71%, and 50%; and 100%, 100%, and 100% at 1, 5, and 9 years, respectively. We concluded that renal angioplasty is a safe and durable modality for treating RAFMD with favorable short and longterm clinical outcomes. Patients with combined atherosclerotic disease and FMD were older and more likely to have declining renal function over time. Early intervention may be imperative to achieve a possible cure of hypertension. Trinquart et al [40] reported his systematic comparison review of 1,616 patients in 47 renal artery angioplasty studies and 1,014 patients in 23 open surgery studies. The cure from malignant hypertension in the angioplasty group was estimated to be 46% (95% confidence interval, 40%52%) compared with 58% (95% confidence interval, 53%62%) in the open surgery group. These results highlight the efficacy and compatibility of angioplasty in patients with symptomatic
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renal artery stenosis. All respected authorities agree that the indications for stenting after angioplasty of patients with RAFMD should be limited to flow-limiting dissection, combined atherosclerotic ostial lesions, or persistent pressure gradients across the lesion >30 mm Hg.
2.5.
Open surgery
The role for open surgery in patients with RAFMD is decreasing and current indications include failure of percutaneous therapy and aneurysmal disease where minimally invasive procedures are not an option [23,36,41].
2.6.
Denervation and renal fibromuscular dysplasia
The most recent update in the treatment of patients with recalcitrant hypertension is the advent of renal artery denervation therapy. Radiofrequency ablation within the renal artery can denervate the autonomic circuit, which consists of afferentefferent nerves within the adventitial layers of renal arteries. Early reports from international clinical trials are promising, with a mean BP reduction of 30 mm Hg at 3year follow-up for patients with malignant hypertension [42,43]. This early enthusiasm has led to a clinical trial in the United States. There are some anecdotal reports on the efficacy of renal artery denervation therapy in treating patients with RAFMD [44]. These data are still in their infancy stage and more durable studies are needed before generalizing this therapy as an option for patients with RAFMD.
2.7.
Differential diagnosis
2.7.1.
Atherosclerosis
RAFMD is not atherosclerotic arteriopathy and it can be differentiated from atherosclerotic renal artery disease based on age, as the mean age for RAFMD is at least 2 decades younger than atherosclerotic renal artery disease. Also, lesion characteristics are more ostial and more focal in atherosclerotic renal artery disease;,and usually mid to distal segment and more multifocal in RAFMD. We have demonstrated that patients with combined diseases are older and are more likely to have declining renal function over time [37]. Others have reported the possibility of combined renal pathology in older patients as well [45–47].
2.7.2.
Vasculitis
Although RAFMD is considered a medium-sized arteriopathy, the most distinguished difference between FMD and vasculitis is the absence of acute phase reactants, such as erythrocyte sedimentation rate, C-reactive protein, fibrinogen, α-1 antitrypsin, haptoglobin, interleukin-1 receptor antagonist, hepcidin, ferritin, procalcitonin, and others in patients with RAFMD.
2.7.3.
Standing arterial waves
These are an intraoperative phenomenon that can confuse clinicians between RAFMD and renal artery spasm with string of beads and arterial waves from catheter manipulation within the renal artery, likely secondary to a muscular spasm.
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Clinician experience and the use of intraoperative nitroglycerin may help to distinguish between the two entities [24].
2.7.4.
Segmental arterial mediolysis
This condition presents in a fashion that is similar to medial type FMD and is usually associated with early dissection, focal aneurysmal formation, or even arterial occlusion [48,49].
3.
Conclusions
This report highlights the fact that RAFMD is still an underdiagnosed entity that can affect any arterial bed, mainly at a younger age, but presentation at an older age is common. Also, percutaneous interventions for symptomatic main renal artery RAFMD are safe, feasible, and technically achievable in most patients. Most reports indicate that short- and longterm clinical responses are encouraging and percutaneous angioplasty for symptomatic RAFMD should be considered as the initial intervention. Surgical revascularization might be necessary when FMD is accompanied by large aneurysmal changes, but should otherwise be limited to patients who fail or do not meet the requirements for angioplasty.
re fe r en ces
[1] Pontes Tde C, Rufino GP, Gurgel MG, et al. Fibromuscular dysplasia: a differential diagnosis of vasculitis. Rev Bras Reumatol 2012;52:70–4. [2] Poloskey SL, Kim E, Sanghani R, et al. Low yield of genetic testing for known vascular connective tissue disorders in patients with fibromuscular dysplasia. Vasc Med 2012;17: 371–8. [3] Olin JW, Froehlich J, Gu X, et al. The United States Registry for Fibromuscular Dysplasia: results in the first 447 patients. Circulation 2012;125:3182–90. [4] Harrison EG Jr, Hunt JC, Bernatz PE. Morphology of fibromuscular dysplasia of the renal artery in renovascular hypertension. Am J Med 1967;43:97–112. [5] Rastogi N, Kabutey NK, Kim D, et al. Symptomatic fibromuscular dysplasia of the external iliac artery. Ann Vasc Surg 2012;26:574.e9–13. [6] Cormier F, Cormier JM. [Thirty-eight cases of dysplasia of the superior mesenteric artery]. J Mal Vasc 2005;30:150–61. [7] Sekar N, Shankar R. Fibromuscular dysplasia with multiple visceral artery involvement. J Vasc Surg 2013;57:1401. [8] Saw J, Poulter R, Fung A. Intracoronary imaging of coronary fibromuscular dysplasia with OCT and IVUS. Catheter Cardiovasc Interv 2013;82:E879–83. [9] Yoshimuta T, Akutsu K, Okajima T, et al. Images in cardiovascular medicine. “String of beads” appearance of bilateral brachial artery in fibromuscular dysplasia. Circulation 2008;117: 2542–3. [10] Davies MG, Saad WE, Peden EK, et al. The long-term outcomes of percutaneous therapy for renal artery fibromuscular dysplasia. J Vasc Surg 2008;48:865–71. [11] Slovut DP, Olin JW. Fibromuscular dysplasia. Curr Treatment Options Cardiovasc Med 2005;7:159–69. [12] Slovut DP, Olin JW. Fibromuscular dysplasia. N Engl J Med 2004;350:1862–71. [13] Doody O, Adam WR, Foley PT, et al. Fibromuscular dysplasia presenting with bilateral renal infarction. Cardiovasc Intervent Radiol 2009;32:329–32.
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[14] Sinnamon K, McNally D, Harty J. Fibromuscular dysplasia presenting as renal infarction. Kidney Int 2007;72:1295–6. [15] Stone PA, Campbell JE, Aburahma AF, et al. Ten-year experience with renal artery in-stent stenosis. J Vasc Surg 2011;53:1026–31. [16] Bates MC, Campbell JE, Broce M, et al. Serum creatinine stabilization following renal artery stenting. Vasc Endovasc Surg 2008;42:40–6. [17] Bates MC, Campbell JE, Stone PA, et al. Factors affecting longterm survival following renal artery stenting. Catheter Cardiovasc Interv 2007;69:1037–43. [18] Bates MC, Rashid M, Campbell JE, et al. Factors influencing the need for target vessel revascularization after renal artery stenting. J Endovasc Ther 2006;13:569–77. [19] Bates MC, Crotty B, Kavasmaneck C, et al. Renal artery angiography: "the right ipsilateral oblique" myth. Catheter Cardiovasc Interv 2006;67:283–7. [20] Kaplan NM. Changing hypertension treatment to reduce the overall cardiovascular risk. J Hypertens Suppl 1990;8:S175–9. [21] Edwards JM, Zaccardi MJ, Strandness DE Jr. A preliminary study of the role of duplex scanning in defining the adequacy of treatment of patients with renal artery fibromuscular dysplasia. J Vasc Surg 1992;15:604–9, (discussion 60911). [22] Cragg AH, Smith TP, Thompson BH, et al. Incidental fibromuscular dysplasia in potential renal donors: long-term clinical follow-up. Radiology 1989;172:145–7. [23] Olin JW. Recognizing and managing fibromuscular dysplasia. Cleve Clin J Med 2007;74:273–4, (27782). [24] Olin JW, Gornik HL. Standing waves are not fibromuscular dysplasia. JACC Cardiovasc Interv 2012;5:888, (author reply 8889). [25] Olin JW, Sealove BA. Diagnosis, management, and future developments of fibromuscular dysplasia. J Vasc Surg 2011;53:826–36, e821. [26] Goldblatt H, Haas E, Klick RL, et al. The effect of main artery occlusion of one kidney on blood pressure of dogs. Proc Natl Acad Sci U S A 1976;73:1722–4. [27] Alhaj EK, Alhaj NK, Klapholz M. Fibromuscular dysplasia of the renal artery: an underdiagnosed cause of severe hypertension. Int J Cardiol 2013;167:e159–60. [28] Kim ES, Olin JW, Froehlich JB, et al. Clinical manifestations of fibromuscular dysplasia vary by patient sex: a report of the United States registry for fibromuscular dysplasia. J Am Coll Cardiol 2013;62:2026–8. [29] Olin JW, Piedmonte MR, Young JR, et al. The utility of duplex ultrasound scanning of the renal arteries for diagnosing significant renal artery stenosis. Ann Intern Med 1995;122:833–8. [30] McKenzie GA, Oderich GS, Kawashima A, et al. Renal artery fibromuscular dysplasia in 2,640 renal donor subjects: a CT angiography analysis. J Vasc Intervent Radiol 2013;24:1477–80. [31] Savard S, Steichen O, Azarine A, et al. Association between 2 angiographic subtypes of renal artery fibromuscular dysplasia and clinical characteristics. Circulation 2012;126:3062–9. [32] Clemente A, Macchi V, Porzionato A, et al. CTA and 2D-3D post-processing: radiological signs of fibromuscular dysplasia of renal artery. Surg Radiol Anat 2009;31:25–9. [33] Basile C, Lisi P, Chimienti D, et al. Fibromuscular dysplasia of renal arteries presenting with bilateral renal infarction in a young man. J Nephrol 2013;26:945–8. [34] Sugiura T, Imoto K, Uchida K, et al. Fibromuscular dysplasia associated with simultaneous spontaneous dissection of four peripheral arteries in a 30-year-old man. Ann Vasc Surg 2011;25: 838. e9–e11. [35] Sciacca L, Ciocca RG, Eslami MH, et al. Endovascular treatment of renal artery aneurysm secondary to fibromuscular dysplasia: a case report. Ann Vasc Surg 2009;23: 536. e912. [36] De Martino RR, Stone DH. Repair of multiple right renal artery aneurysms with associated fibromuscular dysplasia in a solitary kidney. J Vasc Surg 2009;49:497.
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[37] Mousa AY, Campbell JE, Stone PA, et al. Short- and long-term outcomes of percutaneous transluminal angioplasty/stenting of renal fibromuscular dysplasia over a ten-year period. J Vasc Surg 2012;55:421–7. [38] Poloskey SL, Olin JW, Mace P, et al. Fibromuscular dysplasia. Circulation 2012;125:e636–9. [39] Hundae AY, Hebert CA, Schussler JM. Fibromuscular dysplasia of the renal artery as a cause of secondary hypertension. Proc (Bayl Univ Med Cent) 2013;26:405–6. [40] Trinquart L, Mounier-Vehier C, Sapoval M, et al. Efficacy of revascularization for renal artery stenosis caused by fibromuscular dysplasia: a systematic review and meta-analysis. Hypertension 2010;56:525–32. [41] Hirsch AT, Haskal ZJ, Hertzer NR, et al. ACC/AHA 2005 guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): executive summary a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease) endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and
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[43]
[44] [45]
[46]
[47] [48]
[49]
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Vascular Disease Foundation. J Am Coll Cardiol 2006;47: 1239–312. Fadl Elmula FE, Hoffmann P, Fossum E, et al. Renal sympathetic denervation in patients with treatmentresistant hypertension after witnessed intake of medication before qualifying ambulatory blood pressure. Hypertension 2013;62:526–532. Esler MD, Krum H, Sobotka PA, et al. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial. Lancet 2010;376:1903–9. Kelle S, Teller DC, Fleck E, et al. Renal denervation in fibromuscular dysplasia. BMJ Case Rep 2013 Aug 19; 2013. Jayawardene S, Reidy J, Scoble J. Clinical picture: ipsilateral atherosclerotic and fibromuscular renal artery stenosis. Lancet 2000;356:2138. Aqel R, Gupta R, Zoghbi G. Coexistent fibromuscular dysplasia and atherosclerotic renal artery stenosis. J Invasive Cardiol 2005;17:572–3. Pascual A, Bush HS, Copley JB. Renal fibromuscular dysplasia in elderly persons. Am J Kidney Dis 2005;45:e63–6. Slavin RE. Segmental arterial mediolysis: course, sequelae, prognosis, and pathologic-radiologic correlation. Cardiovasc Pathol 2009;18:352–60. Slavin RE, Saeki K, Bhagavan B, et al. Segmental arterial mediolysis: a precursor to fibromuscular dysplasia? Mod Pathol 1995;8:287–94.
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Available online at www.sciencedirect.com
www.elsevier.com/locate/semvascsurg
Renal fibromuscular dysplasia Albeir Y. Mousan, and Gurpreet Gill Department of Surgery, R. C. Byrd Health Sciences Center, West Virginia University, 3110 MacCorkle Avenue SE, Charleston, WV 25304
article info
abstra ct Renal artery fibromuscular dysplasia is a noninflammatory, nonatherosclerotic vasculopathy that can affect renal arteries at various degrees with different severity. The etiology is still unknown, but there is a strong belief that a genetic disorder is the main cause for the pathogenesis of this disease. The main presentation is a sudden onset of recalcitrant hypertension at a young age, which is usually resistant to medical treatment. Once renal artery fibromuscular dysplasia is suspected, several diagnostic tools are available to make an accurate diagnosis. The advent of minimally invasive interventions has revolutionized the options for treatment. This update should provide the clinician with a base understanding of available evidence for diagnosing and treating renal artery fibromuscular dysplasia. & 2014 Elsevier Inc. All rights reserved.
1.
Introduction
Fibromuscular dysplasia (FMD) is a nonatherosclerotic, noninflammatory arterial wall disease that typically affects small- to medium-sized vessels. Despite many theories, the etiology of renal artery fibromuscular dysplasia (RAFMD) remains unknown (Fig 1). All respected authorities agree that a genetic component plays an important role in this disease because it mostly affects Caucasians. In addition, an association between RAFMD and the HLA-DRw6 histocompatibility antigen has also been described [1,2]. FMD occurs predominately in middle-aged females, but it can also affect male patients at different age spectrums. The most common nonatherosclerotic disease related to renovascular hypertension is RAFMD, which accounts for o10% of patients with symptomatic renal artery stenosis. FMD is not exclusive to the renal arteries, it can also affect the extracranial carotid arteries at the same frequency [3], the external iliac arteries (Fig 2) [4,5], and even mesenteric arterial involvement has been reported [6,7]. Coronary vessel involvement with FMD can also occur and can predispose to dissection [8].
n
Corresponding author. E-mail address: [email protected] (A.Y. Mousa).
http://dx.doi.org/10.1053/j.semvascsurg.2014.06.006 0895-7967/$ - see front matter & 2014 Elsevier Inc. All rights reserved.
There are three main pathologic appearances for RAFMD; medial dysplasia is the most common type, accounting for almost 80% of cases. The most characteristic angiographic appearance for the medial type is the “string of beads” appearance [9], as demonstrated in Figure 1. The other two types of RAFMD are intimal fibroplasia and adventitial fibroplasia. The right main renal artery is more commonly affected by RAFMD, but bilateral vessel involvement can occur in up to 35% of patients [10]. Anatomical outcomes of RAFMD include stenosis, occlusion, or aneurysmal formation. The main physiologic concern in patients with RAFMD is uncontrolled hypertension; however, unlike atherosclerotic renal artery disease, RAFMD is rarely associated with loss of renal function, although loss of renal mass can occur in up to 63% of patients [11,12]. Progression of stenosis can occur in up to 37% of patients [12], yet renal artery occlusion with subsequent parenchymal infarct is rare [13,14]. The nature of the disease progression, along with minimal effects on renal function, have encouraged some vascular specialists to recommend medical treatment only as the initial therapy for patients with RAFMD.
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Fig. 1 – Renal artery angiogram showing typical angiographic “string of beads” appearance of fibromuscular dysplasia. Although questioned recently, patients with recalcitrant hypertension may benefit from renal artery angioplasty and stenting, and endovascular treatment with angioplasty has been widely accepted as the standard of care. We previously reported our extensive experience with renal artery stenting for atherosclerotic lesions [15,16].
2.
Clinical presentation
Most patients with RAFMD are asymptomatic, but the most common presentation in symptomatic patients is severe hypertension. These presentations are directly related to the underlying pathology (ie, stenosis, occlusion, or aneurysm formation). All available epidemiologic studies have confirmed that a hemodynamically significant stenotic lesion of the renal artery is the most common cause of secondary hypertension [17–19]. Nevertheless, the incidence of
Fig. 2 – External iliac artery angiogram showing fibromuscular dysplasia appearance.
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renovascular hypertension in the general population is estimated to be 1% to 3% [20,21]. Out of that population, FMD can affect up to 0.5%, therefore, it is considered the most common cause for secondary hypertension in children and young adults [11,12]. The most common population is women between their 3rd and 6th decades. The prevalence of FMD in the general population is still not well characterized, but there is growing evidence that the prevalence is higher than previously thought. In one study, patients with RAFMD constituted 3.8% of 1,862 patients who had renal artery angiograms [22]. Mean age for diagnosing RAFMD is the 6th decade, and this older age indicates that the disease is still underestimated, however, it can occur in any age group [23– 25]. We recommend that any patient with recalcitrant hypertension with triple antihypertensive therapy, including one diuretic, should be considered for a workup for RAFMD. It is worth mentioning that both main pathologies for renal artery stenosis (ie, atherosclerosis and FMD) can produce similar hemodynamic effects with potential sequelae of recalcitrant hypertension and deterioration of renal function. For a better understanding, we rely significantly on Goldblatt’s model, that is, one-kidney, one clip versus two kidneys, and one clip regarding renovascular hypertension and underlying volume versus sodium changes [26]. The clinical presentation of RAFMD is usually acute onset of recalcitrant hypertension in young patients, predominately in female patients. Because RAFMD is a potentially curable source of hypertension, early diagnosis is imperative to initiate adequate therapy. Unexplained malignant hypertension, especially in young females, should alert clinicians to rule out secondary causes, including RAFMD [27]. Kim et al [28] analyzed a very interesting recent registry of 615 patients with FMD. In that registry, the mean age at diagnosis was 51.9 years. Hypertension and headache were the most prevalent presenting symptoms in that study, with no sex predilection; in the mean time, both hypertension and headache were the most common presenting symptoms, leading to the diagnosis of RAFMD for both sexes. Notably, females were more likely to present with extracranial carotid/ vertebral artery stenosis than men, with a higher chance of pulsatile tinnitus (35% v 9%; P ¼ .0002). In that study, men were more likely to present with signs or symptoms of renal artery involvement, such as flank or abdominal pain, azotemia, and renal infarction (42% v 4%; P ¼ .006). In the entire cohort, renal and extracranial vessel involvements were more common than other arterial involvement (7% and 72%). Men were more likely to have RAFMD than carotid involvement (90% v 74%), and women were more likely to present with extracranial carotid disease (74% v 44%). Generally, dissection/aneurysms were common among patients in that registry with 22% of patients having one or more arterial dissections and 21% of patients having one or more aneurysms. Men were more likely to present with aneurysms than dissections (41% v 20%), and females were more likely to present with dissections (39% v 20%; P ¼ .002). Dissections were more likely to occur at extracranial carotid arteries (16%), followed by vertebral arteries (4.2%) and renal arteries (4%). Although men constituted a minority of 8% in that registry, the main presentations for males were still arterial aneurysms or dissections. Females were more likely to
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present with clinical manifestation related to the extracranial carotid artery.
2.1.
Diagnosis
Diagnosis of RAFMD is predominantly dependent on angiographic characteristics of lesions, as arterial tissue samples are rarely available. In a contemporary practice, objective evaluation of patients with renovascular hypertension should begin with a renal artery duplex ultrasound that may show signs of renal artery stenosis in the form of an elevated peak systolic velocity and an aliasing effect, along with a size difference between the two kidneys and a possible elevated reno-aortic ratio Z3.5. Details of renal duplex ultrasound is illustrated at different chapter of that edition. The utility of duplex ultrasound (DUS) in patients with RAFMD has been evaluated in a few studies. Olin et al [29] reported an overall sensitivity of DUS compared with arteriography of 0.98, a specificity of 0.98, a positive predictive value of 0.99, and a negative predictive value of 0.97. The authors concluded that DUS scanning of the renal arteries is an ideal initial screening test, as it is noninvasive and correlates accurately with the degree of renal artery stenosis [29]. However, DUS is an operator-dependent test and can be technically challenging when it comes to evaluating the mid to distal arterial segment. Turbulence, a noisy velocity shift along the arterial segment or beadings on the longitudinal image, can raise suspicion for RAFMD. The diagnosis can be confirmed by a multidetector computed tomography (CT) scan [15] and magnetic resonance angiography [16]. CT angiography plays an important role as well. A recent report from the Mayo Clinic evaluated the incidence, demographics, and clinical presentation of patients diagnosed with RAFMD during a 12-year period using the living donor renal protocol. Of 2,640 patients, 68 were diagnosed with RAFMD (2.6%, 59 were female). The mean age was 52 years and it occurred bilaterally in 32% of patients [30]. An interesting recent retrospective cross-sectional study evaluated the clinical relevance of a binary angiographic classification of RAFMD lesions, either unifocal or multifocal (Z2 focal stenosis), based on CT angiography or magnetic resonance angiography. The interesting conclusion of that study is that the phenotype of the lesion determined the clinical outcomes. Of 337 patients, 82% were multifocal and that group was older (median age of 49 v 30 years), they presented with hypertension at an older age, it was more dominant in females, and fewer had bilateral disease (38% v 79%) [31]. Magnetic resonance angiography and computed tomography angiography are still limited and cannot accurately diagnose any segmental or subsegmental vessel disease. In addition, magnetic resonance angiography might also be limited by motion artifact and can overestimate lesions. To date, subtraction angiography with intravascular ultrasound (IVUS) is the most accurate method for diagnosing RAFMD, demonstrating a classic “string of beads” appearance for the medial type or focal narrowing for the intimal type of RAFMD [32]. We believe that the single most important advancement that has occurred in the world of diagnostic renal tools is the
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development of IVUS (Fig 3). Adding IVUS to renal angiography will minimize the inherited limitations of angiography regarding the hemodynamic effects of the lesions. Also, the use of pressure gradients is controversial because the webs associated with FMD can be “compressed” with a catheter or “pressure wire,” and this may cause a false-negative reading. Additionally, there could be a flow-mediated impact on downstream tissue that is independent of the gradient. However, IVUS gives an accurate understanding of the severity of the stenosis and assists in accurate sizing of balloons. Also, utilizing IVUS to evaluate restenosis after endovascular therapy for RAFMD can be extremely valuable.
2.2.
Fate
RAFMD can cause nonatheromatous arterial stenosis with webs or segmental arterial constrictions that may contribute to parenchymal infarction as an initial presentation [33]. Dissection has been reported as a possible presentation of or outcome for patients with RAFMD [34]. Renal artery aneurysms may occur and the recommended treatment is a covered stent or open surgical repair [35,36].
2.3.
Treatments
When intervention is indicated for patients with recalcitrant hypertension, renal artery angioplasty with or without stenting is currently the most widely recommended initial treatment. Many authors, including our group, have reported on their long-term experience with renal artery stenting for atherosclerotic lesions [17–19]. When it comes to RAFMD, only a handful of studies have analyzed the long-term outcomes after endovascular interventions for symptomatic patients [3,10,37]. Although there is no recommended surgical treatment for asymptomatic RAFMD, these patients should be given antiplatelets and statin therapy, if not contraindicated [25]. The appropriate treatment should be offered to all patients with symptomatic RAFMD [1,38].
Fig. 3 – Intravascular ultrasound (IVUS) demonstration of intravascular appearance of fibromuscular dysplasia— web-like projection—including chromo IVUS [4]. (Color version of figure is available online.)
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Endovascular therapy
Balloon angioplasty has been shown to be successful by disrupting the “webs" of tissue in the renal artery [39]. Percutaneous intervention for symptomatic RAFMD has replaced surgical therapy as the first line of treatment [10]. In our recent publication [37], we evaluated the short- and long-term outcomes of percutaneous transluminal intervention in patients with symptomatic renal artery stenosis due to RAFMD and/or the combination of RAFMD with aorto-ostial atherosclerotic disease. A retrospective analysis was conducted for all patients with RAFMD who underwent transcatheter therapy during a 10-year period. Blood pressure (BP) measurement, the number of BP medications, and hypertension as defined by systolic BP >140 mm Hg and/or diastolic BP >90 mm Hg were recorded. Renal function was defined by an estimated glomerular filtration rate (eGFR). Restenosis was defined by stenosis >60% as determined by renal artery duplex and/or angiography. Freedom from events (ie, restenosis, renal failure, or recurrent hypertension) was performed using a life-table analysis. We examined 43 procedures in 35 patients with RAFMD. Thirty-two patients (91%) were women, with a mean age of 61.9 years. The technical success rate was 100%, with adjunctive stent placement required in the FMD segment for dissection in one patient (2.3%) and in the nonFMD aorto-ostial atherosclerotic lesion in four patients (9.3%). Short-term outcomes were the following: the majority (69%) had an immediate clinical benefit for hypertension, 63% improved with less than or equal to preoperative BP medications, and 6% were cured without BP medications. Postintervention, 17% remained at a moderately reduced renal function (o60 mL/min), and the percentage >60 mL/min eGFR increased significantly (from 51% to 69%; P ¼ .002). For the entire cohort, renal function (mean eGFR) increased significantly from 71.9 mL/min þ 5.8 to 80.8 mL/min þ 5.2; P ¼ .007). Long-term outcomes were the following: freedom from recurrent or worsening hypertension (>140 mm Hg systolic BP and >90 mm Hg diastolic BP) was 93%, 75%, and 41%; and freedom from reduced renal function (eGFR o30 mL/minute) was 100%, 95%, and 64% at 1, 5, and 8 years, respectively. Patients with reduced baseline renal function (o60 mL/min) and combined atherosclerotic disease were more likely to experience long-term reduced renal function (eGFR o30 mL/min; P ¼ .003). The primary and assisted primary patency rates were 95%, 71%, and 50%; and 100%, 100%, and 100% at 1, 5, and 9 years, respectively. We concluded that renal angioplasty is a safe and durable modality for treating RAFMD with favorable short and longterm clinical outcomes. Patients with combined atherosclerotic disease and FMD were older and more likely to have declining renal function over time. Early intervention may be imperative to achieve a possible cure of hypertension. Trinquart et al [40] reported his systematic comparison review of 1,616 patients in 47 renal artery angioplasty studies and 1,014 patients in 23 open surgery studies. The cure from malignant hypertension in the angioplasty group was estimated to be 46% (95% confidence interval, 40%52%) compared with 58% (95% confidence interval, 53%62%) in the open surgery group. These results highlight the efficacy and compatibility of angioplasty in patients with symptomatic
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renal artery stenosis. All respected authorities agree that the indications for stenting after angioplasty of patients with RAFMD should be limited to flow-limiting dissection, combined atherosclerotic ostial lesions, or persistent pressure gradients across the lesion >30 mm Hg.
2.5.
Open surgery
The role for open surgery in patients with RAFMD is decreasing and current indications include failure of percutaneous therapy and aneurysmal disease where minimally invasive procedures are not an option [23,36,41].
2.6.
Denervation and renal fibromuscular dysplasia
The most recent update in the treatment of patients with recalcitrant hypertension is the advent of renal artery denervation therapy. Radiofrequency ablation within the renal artery can denervate the autonomic circuit, which consists of afferentefferent nerves within the adventitial layers of renal arteries. Early reports from international clinical trials are promising, with a mean BP reduction of 30 mm Hg at 3year follow-up for patients with malignant hypertension [42,43]. This early enthusiasm has led to a clinical trial in the United States. There are some anecdotal reports on the efficacy of renal artery denervation therapy in treating patients with RAFMD [44]. These data are still in their infancy stage and more durable studies are needed before generalizing this therapy as an option for patients with RAFMD.
2.7.
Differential diagnosis
2.7.1.
Atherosclerosis
RAFMD is not atherosclerotic arteriopathy and it can be differentiated from atherosclerotic renal artery disease based on age, as the mean age for RAFMD is at least 2 decades younger than atherosclerotic renal artery disease. Also, lesion characteristics are more ostial and more focal in atherosclerotic renal artery disease;,and usually mid to distal segment and more multifocal in RAFMD. We have demonstrated that patients with combined diseases are older and are more likely to have declining renal function over time [37]. Others have reported the possibility of combined renal pathology in older patients as well [45–47].
2.7.2.
Vasculitis
Although RAFMD is considered a medium-sized arteriopathy, the most distinguished difference between FMD and vasculitis is the absence of acute phase reactants, such as erythrocyte sedimentation rate, C-reactive protein, fibrinogen, α-1 antitrypsin, haptoglobin, interleukin-1 receptor antagonist, hepcidin, ferritin, procalcitonin, and others in patients with RAFMD.
2.7.3.
Standing arterial waves
These are an intraoperative phenomenon that can confuse clinicians between RAFMD and renal artery spasm with string of beads and arterial waves from catheter manipulation within the renal artery, likely secondary to a muscular spasm.
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Clinician experience and the use of intraoperative nitroglycerin may help to distinguish between the two entities [24].
2.7.4.
Segmental arterial mediolysis
This condition presents in a fashion that is similar to medial type FMD and is usually associated with early dissection, focal aneurysmal formation, or even arterial occlusion [48,49].
3.
Conclusions
This report highlights the fact that RAFMD is still an underdiagnosed entity that can affect any arterial bed, mainly at a younger age, but presentation at an older age is common. Also, percutaneous interventions for symptomatic main renal artery RAFMD are safe, feasible, and technically achievable in most patients. Most reports indicate that short- and longterm clinical responses are encouraging and percutaneous angioplasty for symptomatic RAFMD should be considered as the initial intervention. Surgical revascularization might be necessary when FMD is accompanied by large aneurysmal changes, but should otherwise be limited to patients who fail or do not meet the requirements for angioplasty.
re fe r en ces
[1] Pontes Tde C, Rufino GP, Gurgel MG, et al. Fibromuscular dysplasia: a differential diagnosis of vasculitis. Rev Bras Reumatol 2012;52:70–4. [2] Poloskey SL, Kim E, Sanghani R, et al. Low yield of genetic testing for known vascular connective tissue disorders in patients with fibromuscular dysplasia. Vasc Med 2012;17: 371–8. [3] Olin JW, Froehlich J, Gu X, et al. The United States Registry for Fibromuscular Dysplasia: results in the first 447 patients. Circulation 2012;125:3182–90. [4] Harrison EG Jr, Hunt JC, Bernatz PE. Morphology of fibromuscular dysplasia of the renal artery in renovascular hypertension. Am J Med 1967;43:97–112. [5] Rastogi N, Kabutey NK, Kim D, et al. Symptomatic fibromuscular dysplasia of the external iliac artery. Ann Vasc Surg 2012;26:574.e9–13. [6] Cormier F, Cormier JM. [Thirty-eight cases of dysplasia of the superior mesenteric artery]. J Mal Vasc 2005;30:150–61. [7] Sekar N, Shankar R. Fibromuscular dysplasia with multiple visceral artery involvement. J Vasc Surg 2013;57:1401. [8] Saw J, Poulter R, Fung A. Intracoronary imaging of coronary fibromuscular dysplasia with OCT and IVUS. Catheter Cardiovasc Interv 2013;82:E879–83. [9] Yoshimuta T, Akutsu K, Okajima T, et al. Images in cardiovascular medicine. “String of beads” appearance of bilateral brachial artery in fibromuscular dysplasia. Circulation 2008;117: 2542–3. [10] Davies MG, Saad WE, Peden EK, et al. The long-term outcomes of percutaneous therapy for renal artery fibromuscular dysplasia. J Vasc Surg 2008;48:865–71. [11] Slovut DP, Olin JW. Fibromuscular dysplasia. Curr Treatment Options Cardiovasc Med 2005;7:159–69. [12] Slovut DP, Olin JW. Fibromuscular dysplasia. N Engl J Med 2004;350:1862–71. [13] Doody O, Adam WR, Foley PT, et al. Fibromuscular dysplasia presenting with bilateral renal infarction. Cardiovasc Intervent Radiol 2009;32:329–32.
R G E R Y
26 (2013) 213–218
217
[14] Sinnamon K, McNally D, Harty J. Fibromuscular dysplasia presenting as renal infarction. Kidney Int 2007;72:1295–6. [15] Stone PA, Campbell JE, Aburahma AF, et al. Ten-year experience with renal artery in-stent stenosis. J Vasc Surg 2011;53:1026–31. [16] Bates MC, Campbell JE, Broce M, et al. Serum creatinine stabilization following renal artery stenting. Vasc Endovasc Surg 2008;42:40–6. [17] Bates MC, Campbell JE, Stone PA, et al. Factors affecting longterm survival following renal artery stenting. Catheter Cardiovasc Interv 2007;69:1037–43. [18] Bates MC, Rashid M, Campbell JE, et al. Factors influencing the need for target vessel revascularization after renal artery stenting. J Endovasc Ther 2006;13:569–77. [19] Bates MC, Crotty B, Kavasmaneck C, et al. Renal artery angiography: "the right ipsilateral oblique" myth. Catheter Cardiovasc Interv 2006;67:283–7. [20] Kaplan NM. Changing hypertension treatment to reduce the overall cardiovascular risk. J Hypertens Suppl 1990;8:S175–9. [21] Edwards JM, Zaccardi MJ, Strandness DE Jr. A preliminary study of the role of duplex scanning in defining the adequacy of treatment of patients with renal artery fibromuscular dysplasia. J Vasc Surg 1992;15:604–9, (discussion 60911). [22] Cragg AH, Smith TP, Thompson BH, et al. Incidental fibromuscular dysplasia in potential renal donors: long-term clinical follow-up. Radiology 1989;172:145–7. [23] Olin JW. Recognizing and managing fibromuscular dysplasia. Cleve Clin J Med 2007;74:273–4, (27782). [24] Olin JW, Gornik HL. Standing waves are not fibromuscular dysplasia. JACC Cardiovasc Interv 2012;5:888, (author reply 8889). [25] Olin JW, Sealove BA. Diagnosis, management, and future developments of fibromuscular dysplasia. J Vasc Surg 2011;53:826–36, e821. [26] Goldblatt H, Haas E, Klick RL, et al. The effect of main artery occlusion of one kidney on blood pressure of dogs. Proc Natl Acad Sci U S A 1976;73:1722–4. [27] Alhaj EK, Alhaj NK, Klapholz M. Fibromuscular dysplasia of the renal artery: an underdiagnosed cause of severe hypertension. Int J Cardiol 2013;167:e159–60. [28] Kim ES, Olin JW, Froehlich JB, et al. Clinical manifestations of fibromuscular dysplasia vary by patient sex: a report of the United States registry for fibromuscular dysplasia. J Am Coll Cardiol 2013;62:2026–8. [29] Olin JW, Piedmonte MR, Young JR, et al. The utility of duplex ultrasound scanning of the renal arteries for diagnosing significant renal artery stenosis. Ann Intern Med 1995;122:833–8. [30] McKenzie GA, Oderich GS, Kawashima A, et al. Renal artery fibromuscular dysplasia in 2,640 renal donor subjects: a CT angiography analysis. J Vasc Intervent Radiol 2013;24:1477–80. [31] Savard S, Steichen O, Azarine A, et al. Association between 2 angiographic subtypes of renal artery fibromuscular dysplasia and clinical characteristics. Circulation 2012;126:3062–9. [32] Clemente A, Macchi V, Porzionato A, et al. CTA and 2D-3D post-processing: radiological signs of fibromuscular dysplasia of renal artery. Surg Radiol Anat 2009;31:25–9. [33] Basile C, Lisi P, Chimienti D, et al. Fibromuscular dysplasia of renal arteries presenting with bilateral renal infarction in a young man. J Nephrol 2013;26:945–8. [34] Sugiura T, Imoto K, Uchida K, et al. Fibromuscular dysplasia associated with simultaneous spontaneous dissection of four peripheral arteries in a 30-year-old man. Ann Vasc Surg 2011;25: 838. e9–e11. [35] Sciacca L, Ciocca RG, Eslami MH, et al. Endovascular treatment of renal artery aneurysm secondary to fibromuscular dysplasia: a case report. Ann Vasc Surg 2009;23: 536. e912. [36] De Martino RR, Stone DH. Repair of multiple right renal artery aneurysms with associated fibromuscular dysplasia in a solitary kidney. J Vasc Surg 2009;49:497.
218
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[37] Mousa AY, Campbell JE, Stone PA, et al. Short- and long-term outcomes of percutaneous transluminal angioplasty/stenting of renal fibromuscular dysplasia over a ten-year period. J Vasc Surg 2012;55:421–7. [38] Poloskey SL, Olin JW, Mace P, et al. Fibromuscular dysplasia. Circulation 2012;125:e636–9. [39] Hundae AY, Hebert CA, Schussler JM. Fibromuscular dysplasia of the renal artery as a cause of secondary hypertension. Proc (Bayl Univ Med Cent) 2013;26:405–6. [40] Trinquart L, Mounier-Vehier C, Sapoval M, et al. Efficacy of revascularization for renal artery stenosis caused by fibromuscular dysplasia: a systematic review and meta-analysis. Hypertension 2010;56:525–32. [41] Hirsch AT, Haskal ZJ, Hertzer NR, et al. ACC/AHA 2005 guidelines for the management of patients with peripheral arterial disease (lower extremity, renal, mesenteric, and abdominal aortic): executive summary a collaborative report from the American Association for Vascular Surgery/Society for Vascular Surgery, Society for Cardiovascular Angiography and Interventions, Society for Vascular Medicine and Biology, Society of Interventional Radiology, and the ACC/AHA Task Force on Practice Guidelines (Writing Committee to Develop Guidelines for the Management of Patients With Peripheral Arterial Disease) endorsed by the American Association of Cardiovascular and Pulmonary Rehabilitation; National Heart, Lung, and Blood Institute; Society for Vascular Nursing; TransAtlantic Inter-Society Consensus; and
R G E R Y
[42]
[43]
[44] [45]
[46]
[47] [48]
[49]
26 (2013) 213–218
Vascular Disease Foundation. J Am Coll Cardiol 2006;47: 1239–312. Fadl Elmula FE, Hoffmann P, Fossum E, et al. Renal sympathetic denervation in patients with treatmentresistant hypertension after witnessed intake of medication before qualifying ambulatory blood pressure. Hypertension 2013;62:526–532. Esler MD, Krum H, Sobotka PA, et al. Renal sympathetic denervation in patients with treatment-resistant hypertension (The Symplicity HTN-2 Trial): a randomised controlled trial. Lancet 2010;376:1903–9. Kelle S, Teller DC, Fleck E, et al. Renal denervation in fibromuscular dysplasia. BMJ Case Rep 2013 Aug 19; 2013. Jayawardene S, Reidy J, Scoble J. Clinical picture: ipsilateral atherosclerotic and fibromuscular renal artery stenosis. Lancet 2000;356:2138. Aqel R, Gupta R, Zoghbi G. Coexistent fibromuscular dysplasia and atherosclerotic renal artery stenosis. J Invasive Cardiol 2005;17:572–3. Pascual A, Bush HS, Copley JB. Renal fibromuscular dysplasia in elderly persons. Am J Kidney Dis 2005;45:e63–6. Slavin RE. Segmental arterial mediolysis: course, sequelae, prognosis, and pathologic-radiologic correlation. Cardiovasc Pathol 2009;18:352–60. Slavin RE, Saeki K, Bhagavan B, et al. Segmental arterial mediolysis: a precursor to fibromuscular dysplasia? Mod Pathol 1995;8:287–94.
