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Nutcracker Syndrome
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Nutcracker Syndrome Manju Kalra and Peter Gloviczki
Compression of the left renal vein (LRV) between the superior mesenteric artery (SMA) and the abdominal aorta was first described by Grant in 1937, who found the anatomic relationship analogous to a nut in a nutcracker.1 The first clinical report was by El-Sadr in 1950, although the compression was documented by venography only 2 decades later by Chait.2 The term nutcracker phenomenon was coined by de Schepper in 1972. The importance of retroperitoneal fat in maintaining a wide aortomesenteric angle was suggested by Stavros et al., and classically an asthenic body habitus has since been associated with nutcracker syndrome (NCS) or symptoms secondary to the nutcracker phenomenon (Fig. 22.1). Stretching the LRV secondary to a posteriorly ptotic left kidney, excess fibrous tissue aortomesenteric angle and wasted paraspinal muscles have also been incriminated. The LRV may also be compressed between the aorta and the vertebral body, leading to a description of a posterior NCS by Lau et al. in 1986. The most common symptoms of LRV compression include flank pain and hematuria secondary to the increased venous pressure and development of varices in the renal pelvis that rupture into the urinary collecting system. Other reported symptoms include left-sided varicocele in males, pelvic congestion syndrome in females, orthostatic proteinuria, and chronic fatigue. Diagnosis is difficult, often delayed and made only after ruling out all other causes of hematuria and flank pain. It is established by a combination of cystoscopy, ultrasonography, computed tomography (CT) scan and venography with measurement of pressure gradients between the LRV and the inferior vena cava (IVC).3,4
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Abstract
Keywords
Compression of the left renal vein (LRV) between the superior mesenteric artery (SMA) and the abdominal aorta was first described in 1937 with the anatomical relationship analogous to a nut in a nutcracker. The commonest symptoms of LRV compression include flank pain and hematuria secondary to the increased venous pressure and development of varices in the renal pelvis that rupture into the urinary collecting system. Color duplex ultrasound (DUS) is a good screening study to confirm the presence of anatomical LRV compression. Computed tomography (CT) venography and magnetic resonance imaging scans can also demonstrate the nature and degree of LRV narrowing, retroperitoneal, and renal hilar collaterals. The aim of intervention for NCS is to reduce LRV hypertension. The lack of correlation of symptoms with radiological features makes prediction of operative outcomes difficult. Open, endovascular, and hybrid treatment options are described albeit with limited concentration of experience due to rarity of the disorder. Renal vein transposition is safe and effective and should be considered first-line therapy along with whatever adjuncts, including hybrid repair, are needed to ensure a wide, tension-free anastomosis to the IVC. Hybrid reconstruction combining open repair followed by stenting is an attractive option. The stent is sewn in place to the vein to prevent migration and ensure a better postoperative result. Early results of primary stenting are satisfactory, but long-term outcome results are limited.
nutcracker flank pain hematuria renal vein transposition gonadal vein transposition stent
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Fig. 22.1 Nutcracker syndrome. Left renal vein (LRV) compressed as it passes between the aorta and the superior mesenteric artery (SMA). LRA, Left renal artery. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
DIAGNOSIS Cystoscopy is indicated in all patients with hematuria to rule out other causes and localize the source to the left ureteric orifice. It, however, may be normal or noncontributory in patients with intermittent or no hematuria.
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Duplex Ultrasonography Color duplex ultrasound (DUS) is a good screening study to confirm the presence of anatomic LRV compression and has been used for the diagnosis of LRV compression syndrome since 1986.3,5–7 This should be the initial test if the diagnosis is suspected. However, it has the drawbacks of poor visualization on occasion and operator dependence. A variety of diagnostic criteria have been described. The major ultrasound features are the aortomesenteric angle, aortomesenteric and hilar renal vein anteroposterior (AP) diameter, and peak systolic velocity (PSV) ratios with a ratio greater than 4 : 5 being acceptable to consider the diagnosis (Fig. 22.2). Arima demonstrated symptomatic compression of the LRV when the aortomesenteric angle was less than 6 to 16 degrees (normal around 40 degrees). Other criteria include an AP diameter ratio of 4 and a mean PSV ratio of greater than 5 in patients with symptomatic NCS. However, these vary widely; in a study by Park et al., only 49% of patients had a PSV and AP diameter ratio greater than 4.8 Kim reported a mean PSV ratio of 7.9 ± 2.7 in patients with clinical NCS and 2.8 ± 1.5 in asymptomatic controls.9 They reported 90% sensitivity and 100% specificity to diagnose NCS when the mean of the two ratios (AP diameter and PSV) was greater than 5. Park et al., in a similar study, designated an AP diameter to PSV ratio of 4 to be diagnostic.8 Takebayashi et al. compared DUS with conventional left renal venography and reported sensitivity and specificity of DUS to diagnose NCS of 78% and 100%, respectively, when the color flow in the collateral veins is included in the diagnostic criteria.7
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B Fig. 22.2 Duplex ultrasound images showing the peak systolic velocity (PSV) (A) at the hilar segment of the left renal vein and (B) in the aortomesenteric angle; PSV ratio = 11.3. ■
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Computed Tomography/Magnetic Resonance Imaging/Intravascular Ultrasound CT venography and magnetic resonance imaging (MRI) scans can also demonstrate the nature and degree of LRV narrowing, retroperitoneal, and renal hilar collaterals (Fig. 22.3). A “beak sign” (triangular shape of LRV caused by severe aortomesenteric narrowing) is described. Similar to DUS features, an LRV (hilar-aortomesenteric) diameter ratio cut-off of 4.9 and an angle of less than 41 degrees between the SMA and the aorta are considered diagnostic.10 However, it is imperative that the CT scan be performed specifically to capture the venous phase with maximal distention of the LRV because a CT scan done for other purposes may demonstrate a false-positive compression of the LRV (Fig. 22.4). MRI, although less commonly used, has findings similar to those seen on CT venography. Intravascular ultrasound (IVUS) has also been used to measure the degree of venous stenosis.11 Positive imaging findings of nutcracker phenomenon must always be correlated with the clinical situation.
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Fig. 22.3 Computed tomography venography showing the left renal vein being (LRV) compressed as it passes between the aorta and the superior mesenteric artery (* ). IVC, Inferior vena cava. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.) ■
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B Fig. 22.4 (A) Computed tomography (CT) imaging of the abdomen performed at outside institution reported as nutcracker syndrome, and (B) repeat CT venography to specifically evaluate left renal vein demonstrating no compression. LRV, Left renal vein. ■
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Venography A venous pressure gradient of 2 to 14 mm Hg between the hilar LRV and the IVC during venography has been considered the gold standard for diagnosis, the normal being 0 to 1 mm Hg. Venography also demonstrates narrowing, collaterals, and the nature of venous reflux in the left gonadal vein, as well as direction of flow across the narrowed segment of LRV (Fig. 22.5). However, interpretation of pressure gradients may be fallacious because of high variability in healthy subjects; variation with position, hydration, degree of collateralization, and overlap in values between normal and symptomatic patients. Conversely, postoperative symptom resolution has been reported with no change in pressure gradients.12 Thus radiographic evidence alone is not sufficient to prompt invasive treatment because imaging criteria do not necessarily correlate with symptomatology.12
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B ■ Fig. 22.5 Contrast venography showing (A) narrowing of the left renal vein as it crosses the aorta underneath the superior mesenteric artery (* ), dilatation of the peripheral left renal vein (arrow) and (B) opacification of gonadal, ascending lumbar, adrenal and other collateral veins (arrow).
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PATIENT SELECTION CRITERIA The aim of intervention for NCS is to reduce LRV hypertension. The lack of correlation of symptoms with radiologic features makes prediction of operative outcomes difficult. Imaging is necessary to confirm significant, anatomic LRV compression, but the indications for intervention remain clinical. Our protocol is guided by patient symptoms (Fig. 22.6). Most operative or endovascular procedures are reserved for severe hematuria and/or debilitating flank pain. For those presenting with a varicocele and flank pain, operative treatment resulted in resolution of the pain, but the varicocele recurred in the majority. Hence in patients presenting with a varicocele alone, we advise traditional treatments (gonadal vein coil occlusion or local ligation). Those with mild or atypical symptoms are offered medical/pain management as the first line of treatment. We compared radiologic criteria in patients we treated surgically with those who were managed conservatively based upon clinical presentation and severity of symptoms and found a significant overlap (Table 22.1).12
■ Fig. 22.6 Nutcracker syndrome: proposed diagnostic and management protocol. CT, Computed tomography; IVC, inferior vena cava; LRV, left renal vein; PSV, peak systolic velocity. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.)
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TABLE 22.1 Patient Demographics in 23 Patients With Nutcracker Syndrome
Median age (years) Male/female Left flank pain Hematuria Pelvic varicosities/varicocele Atypical symptoms Mean LRV PSV ratio Mean pressure gradient LRV/IVC (mm Hg)
Surgical Management (N = 11)
Conservative Management (N = 12)
23 (16–43) 4/7 10 7 3 1a 6.6 (2.5–10)b 4 (2–6)c
18 (14–67) 6/6 3 5 6 5a 8.4 (4–12)b 4 (4–5)c
a
Atypical symptoms include bilateral flank pain, postural tachycardia, orthostatic hypotension, painless hematuria, back pain, renal stones, urinary incontinence, weight loss, vomiting, and diarrhea. b Ultrasounds performed in 7 of 11 surgically managed patients; 8 of 12 conservatively managed patients. c Venography performed in 10 of 11 surgically managed patients; 4 of 12 conservatively managed patients. IVC, Inferior vena cava; LRV, left renal vein; PSV, peak systolic velocity. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.)
TREATMENT Open, endovascular, and hybrid treatment options are described albeit with limited concentration of experience because of rarity of the disorder.
Open Reconstruction Left Renal Vein Transposition Left renal vein transposition: Because the basic pathology responsible for NCSs is compression of the renal vein, direct procedures on the LRV are likely to be most efficacious with least risk to other structures. This is the most common and most effective procedure in which the LRV is transposed distally onto the IVC at an area where the aortomesenteric space is wider (Fig. 22.7). Through a transabdominal, transperitoneal minilaparotomy, the small bowel is retracted to the right and in part toward the distal abdomen. The retroperitoneum is opened between the fourth part of the duodenum and the inferior mesenteric vein, in front of the infrarenal abdominal aorta. The LRV is mobilized, and the left adrenal and descending left lumbar vein are ligated and divided to facilitate adequate mobilization. The left gonadal vein is preferably preserved for subsequent coiling to treat unresolved pelvic congestion or as a conduit for bailout secondary procedures. Intraoperative measurement of the pressure gradient can be performed before transecting the LRV. Following systemic heparinization, the IVC is controlled with a side-biting Satinsky clamp across the LRV confluence. The LRV is then transected and a tension-free end-to-side reanastomosis to the IVC at a more distal location is performed. The original insertion site on the IVC is oversewn. Following restoration of flow, patency may be documented with intraoperative DUS, IVUS, or venography.
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B Fig. 22.7 Left renal vein transposition. (A) Illustration showing inferior vena cava (IVC) control, transection of left renal vein, tension-free, end-to-side reanastomosis to the IVC at a distal location and oversewing of the IVC (B) Intraoperative images demonstrating the same. LRA, Left renal artery, LRV, left renal vein; SMA, superior mesenteric artery. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
Left renal vein transposition with patch venoplasty: Permanent distortion of the vein with sclerosis and fixed narrowing of the venous lumen, akin to that seen in the subclavian vein in venous thoracic outlet syndrome, may be present with chronic compression. In patients with a stretched out LRV (ptotic kidney/lack of retroperitoneal fat), a tension-free anastomosis may not be possible once the LRV is transected. A great
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saphenous vein (GSV) patch across the anterior wall of the anastomosis to augment the LRV−IVC confluence after LRV transposition is a useful adjunct (Fig. 22.8). Left renal vein transposition with saphenous vein cuff: In circumstances where the LRV length is totally inadequate to transpose to a sufficiently wide area of the aortomesenteric space, a GSV cuff extension to the LRV may be performed to ensure a
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B Fig. 22.8 Left renal vein transposition with patch venoplasty. (A) Illustration showing a great saphenous vein patch across the anterior wall of the left renal vein–inferior vena cava (LRV-IVC) anastomosis to augment the LRV-IVC confluence after LRV transposition. (B) Intraoperative images demonstrating the same. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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tension-free anastomosis. The GSV cuff is created and first sutured to the IVC with a continuous polypropylene suture following which it is anastomosed end-to-end to the LRV with interrupted 5 or 6 polypropylene sutures (Fig. 22.9). Stenosis or thrombosis of the transposed LRV can occur with recurrence of symptoms. The predisposing causes are a scarred distorted vein, especially one with previous thrombosis with inadequate length to perform a tension-free anastomosis to the IVC.13 Venous Bypass Procedures In patients who have compression of a retroaortic LRV or in those with chronic LRV thrombosis, anterior transposition alone may not be sufficient, and an interposition graft or implantation of the gonadal vein to the IVC may be better alternatives.
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B Fig. 22.9 Left renal vein transposition with saphenous vein cuff. (A) Illustration showing great saphenous vein cuff extension to elongate the left renal vein. (B) Intraoperative image demonstrating the same. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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Gonadal vein transposition: In this technique, the left gonadal vein is transected and reimplanted into the IVC (Fig. 22.10). This is a particularly suitable alternative in patients with NCS and an incompetent left gonadal vein with symptomatic pelvic congestion, or in the setting of thrombosis of the LRV, either de novo or following transposition. This also serves the purpose of decompressing the LRV through the gonadal vein without actual transection and translocation of the LRV itself. The left gonadal vein is approached through the transverse mesocolon similar to the exposure used for LRV transposition. The side branches of the gonadal vein are ligated and divided. The gonadal vein is ligated distally, divided and tunneled under the inferior mesenteric vessels over the abdominal aorta toward the IVC. Following systemic heparinization, the IVC is controlled with a side-biting Satinsky clamp and an end-to-side anastomosis using interrupted 6 polypropylene sutures is performed.
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B Fig. 22.10 Left gonadal vein transposition. (A) Illustration. (B) Intraoperative images showing the vein isolation, distal transection, tunneled under the inferior mesenteric vessels and reimplantation into the inferior vena cava. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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Renocaval great saphenous vein bypass: In the absence of a large-caliber, refluxing gonadal vein, a GSV conduit can be used to bypass the compressed segment of the LRV without the need for transection and transposition (Fig. 22.11). This is an excellent option especially when the compressed segment of LRV has suffered thrombosis as well. Renal autotransplantation: This is a potentially more complete procedure but has the advantage of correcting concomitant posterior ptosis. It involves a much more extensive dissection, longer period of renal ischemia, and additional renal artery and ureteric anastomoses with their attendant risk of complications. It is, however, worth considering as a bailout in the setting of failed prior operative procedures before resorting to nephrectomy in these young patients.
Other Procedures In patients who have fibrous or fibrolymphatic tissue in the etiology of renal vein compression, excision of this tissue may provide immediate relief.14 Anterior or anteromedial
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B Fig. 22.11 Left renal vein stent. (A) Illustration. (B) Intraoperative images, stent placed from the first division of the renal vein. (From Erben Y, Gloviczki P, Kalra M, et.al. Treatment of nutcracker syndrome with open and endovascular interventions. J Vasc Surg Venous Lymphat Disord. 2015;3(4),389–396.) ■
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nephroplexy has been used successfully in patients with posterior ptosis.15,16 Other open operative procedures reported include transposition or bypass of the SMA,17 external stenting of the LRV using ringed polytetrafluoroethylene (PTFE),11,18 and placement of a wedge of Dacron to increase the mesoaortic angle.14 SMA transposition, rarely performed now, incurs the added risks of bowel ischemia and has been reported only rarely. Both the external stent and the wedge have the potential to cause kinking of the SMA in thin patients and risks possible erosion of the Dacron into the bowel. Posterior Nutcracker Syndrome Anterior transposition of the left renal vein: The posterior NCS can be repaired by transposing the retroaortic LRV from its original course to be anterior to the aorta and reimplanting it onto the IVC. The operative technique is similar to that used for the anterior NCS. A retroaortic LRV is more friable and frequently has multiple small tributaries. It may be associated with larger lymph vessels, which require careful ligation to avoid lymphatic leak. The vein is then translocated anterior and cephalad for a tension-free reimplantation into the IVC. The anastomosis can be performed in a continuous fashion to the posterior wall and with interrupted sutures for the anterior wall. If further widening of the LRV is indicated, an incision is made in the anterior wall of the LRV and the anterior wall of the IVC. A vein (GSV) patch is sewn in with a continuous 6 polypropylene suture. GSV patches or cuffs will be frequently required to provide adequate length for successful anterior transposition.
Endovascular Treatment Following work published by Neste et al. in 1996, endovascular options have emerged as an alternative treatment option for NCS. Stents with high radial strength, good conformability, and minimal shortening with deployment systems that allow accurate placement are ideal. In the absence of availability of dedicated venous stents, self-expanding stents (Wallstent, SMART stent) are commonly used. Oversizing is recommended and a 6-cm or longer stent is placed, extending from the first division of the renal vein centrally to the IVC to minimize the risk of migration, the most common complication (see Fig. 22.11). Embolization of the stent to the lung has been reported. Stent protrusion into the IVC is a common observation, but it does not seem to cause any complication. Factors affecting stent migration may include a shorter distance between the ostium and the first large branch of the LRV, the increase in the LRV intraluminal pressure, pulsatility, and proximity of the stent to the abdominal aorta. Other complications, such as stent thrombosis, in-stent restenosis, kinking, and fracture are rare; this may be caused by a high-flow rate and endogenous urokinase. Unfortunately, an ideal stent for use specifically in this anatomic situation does not exist, making the results of stenting suboptimal in the long-term in spite of excellent early relief from symptoms reported.18–25 This minimally invasive approach may become the treatment of choice. However, clearly the long-term fate of intrarenal stents in these young patients with the potential associated complications of stenosis, thrombosis, embolization, and erosion remains to be evaluated.
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Hybrid reconstruction, combining open repair followed by stenting, is an attractive option. The stent is sewn in place to the vein to prevent migration and ensure a better postoperative result (Fig. 22.12). This procedure has been recently adopted by us and combines the advantages of transposing the LRV to a more favorable site in the aortomesenteric angle, with the radial force of the stent serving to keep the vein open
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C ■ Fig. 22.12 Hybrid reconstruction. (A) Intraoperative image showing open repair followed by stenting, stent is sewn in place to the vein to prevent migration. (B) Postoperative computed tomography venography following percutaneous left renal vein stenting and (C) axial and sagittal imaging following hybrid reconstruction demonstrating significant widening of aortomesenteric space (arrow) between (B) and (C).
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at the site of anastomosis to the IVC. Durability and clinical outcome will need to be evaluated.
CONCLUSION In patients with suspected NCS, symptom severity may not correlate with imaging parameters. Careful evaluation of clinical symptoms and thorough investigation of radiologic evidence of LRV compression is advisable before recommending surgical/endovascular intervention to obtain the best long-term outcomes. Patients with severe, classic, and chronic symptoms should be offered intervention. Renal vein transposition is safe and effective, and should be considered first-line therapy along with whatever adjuncts, including hybrid repair, needed to ensure a wide, tension-free anastomosis to the IVC. Early results of primary stenting are satisfactory, but long-term outcome results are limited. Both treatment modalities are invaluable in the event of failure of the other modality.
REFERENCES 1. Grant JCB, ed. A method of anatomy, descriptive and deductive. 3rd ed. Baltimore: The Williams and Wilkins company; 1944:822. xxiv. 2. Chait AMK, Fabian CE, Mellins HZ. Vascular impressions on the ureters. Am J Roentgen Rad Ther. 1971;3:729–749. 3. Stavros AT, Sickler KJ, Menter RR. Color duplex sonography of the nutcracker syndrome (aortomesenteric left renal vein compression). J Ultrasound Med. 1994;13(7):569–574. 4. Imamura A, Nakamura M, Maekawa N, et al. [Usefulness of renal CT scan for analysis of nutcracker phenomenon]. Nippon Hinyokika Gakkai Zasshi. 1992;83(11):1861–1865. 5. Wolfish NM, McLaine PN, Martin D. Renal vein entrapment syndrome: frequency and diagnosis—a lesson in conservatism. Clin Nephrol. 1986;26:96–100. 6. Arima MH, Hosokawa S, Ogino T. Ultrasonographically demonstrated nutcraker phenomenon: alternative to angiography. Int Urol Nephrol. 1990;22:3. 7. Takebayashi S, Ueki T, Ikeda N, et al. Diagnosis of the nutcracker syndrome with color Doppler sonography: correlation with flow patterns on retrograde left renal venography. AJR Am J Roentgenol. 1999;172(1):39–43. 8. Park SJ, Lim JW, Cho BS, et al. Nutcracker syndrome in children with orthostatic proteinuria: diagnosis on the basis of Doppler sonography. J Ultrasound Med. 2002;21(1):39–45, quiz 6. 9. Kim SH, Cho SW, Kim HD, et al. Nutcracker syndrome: diagnosis with Doppler US. Radiology. 1996;198(1):93–97. 10. Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42. 11. Barnes RW, Fleisher HL 3rd, Redman JF, et al. Mesoaortic compression of the left renal vein (the so-called nutcracker syndrome): repair by a new stenting procedure. J Vasc Surg. 1988;8(4):415–421. 12. Reed NR, Kalra M, Bower TC, et al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393, discussion 93–94. 13. Erben Y, Gloviczki P, Kalra M, et al. Treatment of nutcracker syndrome with open and endovascular interventions. J Vasc Surg Venous Lymphat Disord. 2015;3(4):389–396. 14. Ariyoshi A, Nagase K. Renal hematuria caused by “nutcracker” phenomenon: a more logical surgical management. Urology. 1990;35(2):168–170. 15. Wendel R, Crawford ED, Hehman K. The “nutcracker” phenomenon: an unusual cause for renal varicosities with hematuria. J Urol. 1980;123:761–763. 16. Lopatkin NA, Morozov AV, Lopatkina LN. Essential renal hemorrhages. Eur Urol. 1978;4:115–119.
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17. Zhang H, Zhang N, Li M, et al. Treatment of six cases of left renal nutcracker phenomenon: surgery and endografting. Chin Med J. 2003;116(11):1782–1784. 18. Scultetus AH, Villavicencio JL, Gillespie DL. The nutcracker syndrome: its role in the pelvic venous disorders. J Vasc Surg. 2001;34(5):812–819. 19. Lin WQ, Huang HF, Li M, et al. [Diagnosis and therapy of the nutcracker phenomenon: longterm follow-up]. Zhonghua Wai Ke Za Zhi. 2003;41(12):889–892. 20. Segawa N, Azuma H, Iwamoto Y, et al. Expandable metallic stent placement for nutcracker phenomenon. Urology. 1999;53(3):631–633. 21. Park YB, Lim SH, Ahn JH, et al. Nutcracker syndrome: intravascular stenting approach. Nephrol Dial Transplant. 2000;15(1):99–101. 22. Neste MG, Narasimham DL, Belcher KK. Endovascular stent placement as a treatment for renal venous hypertension. J Vasc Interv Radiol. 1996;7(6):859–861. 23. Kim SJ, Kim CW, Kim S, et al. Long-term follow-up after endovascular stent placement for treatment of nutcracker syndrome. J Vasc Interv Radiol. 2005;16(3):428–431. 24. Hartung O, Grisoli D, Boufi M, et al. Endovascular stenting in the treatment of pelvic vein congestion caused by nutcracker syndrome: lessons learned from the first five cases. J Vasc Surg. 2005;42(2):275–280. 25. Zhang H, Li M, Jin W, et al. The left renal entrapment syndrome: diagnosis and treatment. Ann Vasc Surg. 2007;21(2):198–203.
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Nutcracker Syndrome Manju Kalra and Peter Gloviczki
Compression of the left renal vein (LRV) between the superior mesenteric artery (SMA) and the abdominal aorta was first described by Grant in 1937, who found the anatomic relationship analogous to a nut in a nutcracker.1 The first clinical report was by El-Sadr in 1950, although the compression was documented by venography only 2 decades later by Chait.2 The term nutcracker phenomenon was coined by de Schepper in 1972. The importance of retroperitoneal fat in maintaining a wide aortomesenteric angle was suggested by Stavros et al., and classically an asthenic body habitus has since been associated with nutcracker syndrome (NCS) or symptoms secondary to the nutcracker phenomenon (Fig. 22.1). Stretching the LRV secondary to a posteriorly ptotic left kidney, excess fibrous tissue aortomesenteric angle and wasted paraspinal muscles have also been incriminated. The LRV may also be compressed between the aorta and the vertebral body, leading to a description of a posterior NCS by Lau et al. in 1986. The most common symptoms of LRV compression include flank pain and hematuria secondary to the increased venous pressure and development of varices in the renal pelvis that rupture into the urinary collecting system. Other reported symptoms include left-sided varicocele in males, pelvic congestion syndrome in females, orthostatic proteinuria, and chronic fatigue. Diagnosis is difficult, often delayed and made only after ruling out all other causes of hematuria and flank pain. It is established by a combination of cystoscopy, ultrasonography, computed tomography (CT) scan and venography with measurement of pressure gradients between the LRV and the inferior vena cava (IVC).3,4
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C H A P T E R 2 2 n Nutcracker Syndrome
Abstract
Keywords
Compression of the left renal vein (LRV) between the superior mesenteric artery (SMA) and the abdominal aorta was first described in 1937 with the anatomical relationship analogous to a nut in a nutcracker. The commonest symptoms of LRV compression include flank pain and hematuria secondary to the increased venous pressure and development of varices in the renal pelvis that rupture into the urinary collecting system. Color duplex ultrasound (DUS) is a good screening study to confirm the presence of anatomical LRV compression. Computed tomography (CT) venography and magnetic resonance imaging scans can also demonstrate the nature and degree of LRV narrowing, retroperitoneal, and renal hilar collaterals. The aim of intervention for NCS is to reduce LRV hypertension. The lack of correlation of symptoms with radiological features makes prediction of operative outcomes difficult. Open, endovascular, and hybrid treatment options are described albeit with limited concentration of experience due to rarity of the disorder. Renal vein transposition is safe and effective and should be considered first-line therapy along with whatever adjuncts, including hybrid repair, are needed to ensure a wide, tension-free anastomosis to the IVC. Hybrid reconstruction combining open repair followed by stenting is an attractive option. The stent is sewn in place to the vein to prevent migration and ensure a better postoperative result. Early results of primary stenting are satisfactory, but long-term outcome results are limited.
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Fig. 22.1 Nutcracker syndrome. Left renal vein (LRV) compressed as it passes between the aorta and the superior mesenteric artery (SMA). LRA, Left renal artery. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
DIAGNOSIS Cystoscopy is indicated in all patients with hematuria to rule out other causes and localize the source to the left ureteric orifice. It, however, may be normal or noncontributory in patients with intermittent or no hematuria.
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Duplex Ultrasonography Color duplex ultrasound (DUS) is a good screening study to confirm the presence of anatomic LRV compression and has been used for the diagnosis of LRV compression syndrome since 1986.3,5–7 This should be the initial test if the diagnosis is suspected. However, it has the drawbacks of poor visualization on occasion and operator dependence. A variety of diagnostic criteria have been described. The major ultrasound features are the aortomesenteric angle, aortomesenteric and hilar renal vein anteroposterior (AP) diameter, and peak systolic velocity (PSV) ratios with a ratio greater than 4 : 5 being acceptable to consider the diagnosis (Fig. 22.2). Arima demonstrated symptomatic compression of the LRV when the aortomesenteric angle was less than 6 to 16 degrees (normal around 40 degrees). Other criteria include an AP diameter ratio of 4 and a mean PSV ratio of greater than 5 in patients with symptomatic NCS. However, these vary widely; in a study by Park et al., only 49% of patients had a PSV and AP diameter ratio greater than 4.8 Kim reported a mean PSV ratio of 7.9 ± 2.7 in patients with clinical NCS and 2.8 ± 1.5 in asymptomatic controls.9 They reported 90% sensitivity and 100% specificity to diagnose NCS when the mean of the two ratios (AP diameter and PSV) was greater than 5. Park et al., in a similar study, designated an AP diameter to PSV ratio of 4 to be diagnostic.8 Takebayashi et al. compared DUS with conventional left renal venography and reported sensitivity and specificity of DUS to diagnose NCS of 78% and 100%, respectively, when the color flow in the collateral veins is included in the diagnostic criteria.7
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B Fig. 22.2 Duplex ultrasound images showing the peak systolic velocity (PSV) (A) at the hilar segment of the left renal vein and (B) in the aortomesenteric angle; PSV ratio = 11.3. ■
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Computed Tomography/Magnetic Resonance Imaging/Intravascular Ultrasound CT venography and magnetic resonance imaging (MRI) scans can also demonstrate the nature and degree of LRV narrowing, retroperitoneal, and renal hilar collaterals (Fig. 22.3). A “beak sign” (triangular shape of LRV caused by severe aortomesenteric narrowing) is described. Similar to DUS features, an LRV (hilar-aortomesenteric) diameter ratio cut-off of 4.9 and an angle of less than 41 degrees between the SMA and the aorta are considered diagnostic.10 However, it is imperative that the CT scan be performed specifically to capture the venous phase with maximal distention of the LRV because a CT scan done for other purposes may demonstrate a false-positive compression of the LRV (Fig. 22.4). MRI, although less commonly used, has findings similar to those seen on CT venography. Intravascular ultrasound (IVUS) has also been used to measure the degree of venous stenosis.11 Positive imaging findings of nutcracker phenomenon must always be correlated with the clinical situation.
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Fig. 22.3 Computed tomography venography showing the left renal vein being (LRV) compressed as it passes between the aorta and the superior mesenteric artery (* ). IVC, Inferior vena cava. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.) ■
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B Fig. 22.4 (A) Computed tomography (CT) imaging of the abdomen performed at outside institution reported as nutcracker syndrome, and (B) repeat CT venography to specifically evaluate left renal vein demonstrating no compression. LRV, Left renal vein. ■
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Venography A venous pressure gradient of 2 to 14 mm Hg between the hilar LRV and the IVC during venography has been considered the gold standard for diagnosis, the normal being 0 to 1 mm Hg. Venography also demonstrates narrowing, collaterals, and the nature of venous reflux in the left gonadal vein, as well as direction of flow across the narrowed segment of LRV (Fig. 22.5). However, interpretation of pressure gradients may be fallacious because of high variability in healthy subjects; variation with position, hydration, degree of collateralization, and overlap in values between normal and symptomatic patients. Conversely, postoperative symptom resolution has been reported with no change in pressure gradients.12 Thus radiographic evidence alone is not sufficient to prompt invasive treatment because imaging criteria do not necessarily correlate with symptomatology.12
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B ■ Fig. 22.5 Contrast venography showing (A) narrowing of the left renal vein as it crosses the aorta underneath the superior mesenteric artery (* ), dilatation of the peripheral left renal vein (arrow) and (B) opacification of gonadal, ascending lumbar, adrenal and other collateral veins (arrow).
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PATIENT SELECTION CRITERIA The aim of intervention for NCS is to reduce LRV hypertension. The lack of correlation of symptoms with radiologic features makes prediction of operative outcomes difficult. Imaging is necessary to confirm significant, anatomic LRV compression, but the indications for intervention remain clinical. Our protocol is guided by patient symptoms (Fig. 22.6). Most operative or endovascular procedures are reserved for severe hematuria and/or debilitating flank pain. For those presenting with a varicocele and flank pain, operative treatment resulted in resolution of the pain, but the varicocele recurred in the majority. Hence in patients presenting with a varicocele alone, we advise traditional treatments (gonadal vein coil occlusion or local ligation). Those with mild or atypical symptoms are offered medical/pain management as the first line of treatment. We compared radiologic criteria in patients we treated surgically with those who were managed conservatively based upon clinical presentation and severity of symptoms and found a significant overlap (Table 22.1).12
■ Fig. 22.6 Nutcracker syndrome: proposed diagnostic and management protocol. CT, Computed tomography; IVC, inferior vena cava; LRV, left renal vein; PSV, peak systolic velocity. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.)
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TABLE 22.1 Patient Demographics in 23 Patients With Nutcracker Syndrome
Median age (years) Male/female Left flank pain Hematuria Pelvic varicosities/varicocele Atypical symptoms Mean LRV PSV ratio Mean pressure gradient LRV/IVC (mm Hg)
Surgical Management (N = 11)
Conservative Management (N = 12)
23 (16–43) 4/7 10 7 3 1a 6.6 (2.5–10)b 4 (2–6)c
18 (14–67) 6/6 3 5 6 5a 8.4 (4–12)b 4 (4–5)c
a
Atypical symptoms include bilateral flank pain, postural tachycardia, orthostatic hypotension, painless hematuria, back pain, renal stones, urinary incontinence, weight loss, vomiting, and diarrhea. b Ultrasounds performed in 7 of 11 surgically managed patients; 8 of 12 conservatively managed patients. c Venography performed in 10 of 11 surgically managed patients; 4 of 12 conservatively managed patients. IVC, Inferior vena cava; LRV, left renal vein; PSV, peak systolic velocity. (From Reed NR, Kalra M, Bower TC, et.al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393.)
TREATMENT Open, endovascular, and hybrid treatment options are described albeit with limited concentration of experience because of rarity of the disorder.
Open Reconstruction Left Renal Vein Transposition Left renal vein transposition: Because the basic pathology responsible for NCSs is compression of the renal vein, direct procedures on the LRV are likely to be most efficacious with least risk to other structures. This is the most common and most effective procedure in which the LRV is transposed distally onto the IVC at an area where the aortomesenteric space is wider (Fig. 22.7). Through a transabdominal, transperitoneal minilaparotomy, the small bowel is retracted to the right and in part toward the distal abdomen. The retroperitoneum is opened between the fourth part of the duodenum and the inferior mesenteric vein, in front of the infrarenal abdominal aorta. The LRV is mobilized, and the left adrenal and descending left lumbar vein are ligated and divided to facilitate adequate mobilization. The left gonadal vein is preferably preserved for subsequent coiling to treat unresolved pelvic congestion or as a conduit for bailout secondary procedures. Intraoperative measurement of the pressure gradient can be performed before transecting the LRV. Following systemic heparinization, the IVC is controlled with a side-biting Satinsky clamp across the LRV confluence. The LRV is then transected and a tension-free end-to-side reanastomosis to the IVC at a more distal location is performed. The original insertion site on the IVC is oversewn. Following restoration of flow, patency may be documented with intraoperative DUS, IVUS, or venography.
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B Fig. 22.7 Left renal vein transposition. (A) Illustration showing inferior vena cava (IVC) control, transection of left renal vein, tension-free, end-to-side reanastomosis to the IVC at a distal location and oversewing of the IVC (B) Intraoperative images demonstrating the same. LRA, Left renal artery, LRV, left renal vein; SMA, superior mesenteric artery. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
Left renal vein transposition with patch venoplasty: Permanent distortion of the vein with sclerosis and fixed narrowing of the venous lumen, akin to that seen in the subclavian vein in venous thoracic outlet syndrome, may be present with chronic compression. In patients with a stretched out LRV (ptotic kidney/lack of retroperitoneal fat), a tension-free anastomosis may not be possible once the LRV is transected. A great
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saphenous vein (GSV) patch across the anterior wall of the anastomosis to augment the LRV−IVC confluence after LRV transposition is a useful adjunct (Fig. 22.8). Left renal vein transposition with saphenous vein cuff: In circumstances where the LRV length is totally inadequate to transpose to a sufficiently wide area of the aortomesenteric space, a GSV cuff extension to the LRV may be performed to ensure a
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B Fig. 22.8 Left renal vein transposition with patch venoplasty. (A) Illustration showing a great saphenous vein patch across the anterior wall of the left renal vein–inferior vena cava (LRV-IVC) anastomosis to augment the LRV-IVC confluence after LRV transposition. (B) Intraoperative images demonstrating the same. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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tension-free anastomosis. The GSV cuff is created and first sutured to the IVC with a continuous polypropylene suture following which it is anastomosed end-to-end to the LRV with interrupted 5 or 6 polypropylene sutures (Fig. 22.9). Stenosis or thrombosis of the transposed LRV can occur with recurrence of symptoms. The predisposing causes are a scarred distorted vein, especially one with previous thrombosis with inadequate length to perform a tension-free anastomosis to the IVC.13 Venous Bypass Procedures In patients who have compression of a retroaortic LRV or in those with chronic LRV thrombosis, anterior transposition alone may not be sufficient, and an interposition graft or implantation of the gonadal vein to the IVC may be better alternatives.
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B Fig. 22.9 Left renal vein transposition with saphenous vein cuff. (A) Illustration showing great saphenous vein cuff extension to elongate the left renal vein. (B) Intraoperative image demonstrating the same. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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Gonadal vein transposition: In this technique, the left gonadal vein is transected and reimplanted into the IVC (Fig. 22.10). This is a particularly suitable alternative in patients with NCS and an incompetent left gonadal vein with symptomatic pelvic congestion, or in the setting of thrombosis of the LRV, either de novo or following transposition. This also serves the purpose of decompressing the LRV through the gonadal vein without actual transection and translocation of the LRV itself. The left gonadal vein is approached through the transverse mesocolon similar to the exposure used for LRV transposition. The side branches of the gonadal vein are ligated and divided. The gonadal vein is ligated distally, divided and tunneled under the inferior mesenteric vessels over the abdominal aorta toward the IVC. Following systemic heparinization, the IVC is controlled with a side-biting Satinsky clamp and an end-to-side anastomosis using interrupted 6 polypropylene sutures is performed.
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B Fig. 22.10 Left gonadal vein transposition. (A) Illustration. (B) Intraoperative images showing the vein isolation, distal transection, tunneled under the inferior mesenteric vessels and reimplantation into the inferior vena cava. (From Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42.) ■
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Renocaval great saphenous vein bypass: In the absence of a large-caliber, refluxing gonadal vein, a GSV conduit can be used to bypass the compressed segment of the LRV without the need for transection and transposition (Fig. 22.11). This is an excellent option especially when the compressed segment of LRV has suffered thrombosis as well. Renal autotransplantation: This is a potentially more complete procedure but has the advantage of correcting concomitant posterior ptosis. It involves a much more extensive dissection, longer period of renal ischemia, and additional renal artery and ureteric anastomoses with their attendant risk of complications. It is, however, worth considering as a bailout in the setting of failed prior operative procedures before resorting to nephrectomy in these young patients.
Other Procedures In patients who have fibrous or fibrolymphatic tissue in the etiology of renal vein compression, excision of this tissue may provide immediate relief.14 Anterior or anteromedial
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B Fig. 22.11 Left renal vein stent. (A) Illustration. (B) Intraoperative images, stent placed from the first division of the renal vein. (From Erben Y, Gloviczki P, Kalra M, et.al. Treatment of nutcracker syndrome with open and endovascular interventions. J Vasc Surg Venous Lymphat Disord. 2015;3(4),389–396.) ■
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nephroplexy has been used successfully in patients with posterior ptosis.15,16 Other open operative procedures reported include transposition or bypass of the SMA,17 external stenting of the LRV using ringed polytetrafluoroethylene (PTFE),11,18 and placement of a wedge of Dacron to increase the mesoaortic angle.14 SMA transposition, rarely performed now, incurs the added risks of bowel ischemia and has been reported only rarely. Both the external stent and the wedge have the potential to cause kinking of the SMA in thin patients and risks possible erosion of the Dacron into the bowel. Posterior Nutcracker Syndrome Anterior transposition of the left renal vein: The posterior NCS can be repaired by transposing the retroaortic LRV from its original course to be anterior to the aorta and reimplanting it onto the IVC. The operative technique is similar to that used for the anterior NCS. A retroaortic LRV is more friable and frequently has multiple small tributaries. It may be associated with larger lymph vessels, which require careful ligation to avoid lymphatic leak. The vein is then translocated anterior and cephalad for a tension-free reimplantation into the IVC. The anastomosis can be performed in a continuous fashion to the posterior wall and with interrupted sutures for the anterior wall. If further widening of the LRV is indicated, an incision is made in the anterior wall of the LRV and the anterior wall of the IVC. A vein (GSV) patch is sewn in with a continuous 6 polypropylene suture. GSV patches or cuffs will be frequently required to provide adequate length for successful anterior transposition.
Endovascular Treatment Following work published by Neste et al. in 1996, endovascular options have emerged as an alternative treatment option for NCS. Stents with high radial strength, good conformability, and minimal shortening with deployment systems that allow accurate placement are ideal. In the absence of availability of dedicated venous stents, self-expanding stents (Wallstent, SMART stent) are commonly used. Oversizing is recommended and a 6-cm or longer stent is placed, extending from the first division of the renal vein centrally to the IVC to minimize the risk of migration, the most common complication (see Fig. 22.11). Embolization of the stent to the lung has been reported. Stent protrusion into the IVC is a common observation, but it does not seem to cause any complication. Factors affecting stent migration may include a shorter distance between the ostium and the first large branch of the LRV, the increase in the LRV intraluminal pressure, pulsatility, and proximity of the stent to the abdominal aorta. Other complications, such as stent thrombosis, in-stent restenosis, kinking, and fracture are rare; this may be caused by a high-flow rate and endogenous urokinase. Unfortunately, an ideal stent for use specifically in this anatomic situation does not exist, making the results of stenting suboptimal in the long-term in spite of excellent early relief from symptoms reported.18–25 This minimally invasive approach may become the treatment of choice. However, clearly the long-term fate of intrarenal stents in these young patients with the potential associated complications of stenosis, thrombosis, embolization, and erosion remains to be evaluated.
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Hybrid reconstruction, combining open repair followed by stenting, is an attractive option. The stent is sewn in place to the vein to prevent migration and ensure a better postoperative result (Fig. 22.12). This procedure has been recently adopted by us and combines the advantages of transposing the LRV to a more favorable site in the aortomesenteric angle, with the radial force of the stent serving to keep the vein open
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C ■ Fig. 22.12 Hybrid reconstruction. (A) Intraoperative image showing open repair followed by stenting, stent is sewn in place to the vein to prevent migration. (B) Postoperative computed tomography venography following percutaneous left renal vein stenting and (C) axial and sagittal imaging following hybrid reconstruction demonstrating significant widening of aortomesenteric space (arrow) between (B) and (C).
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at the site of anastomosis to the IVC. Durability and clinical outcome will need to be evaluated.
CONCLUSION In patients with suspected NCS, symptom severity may not correlate with imaging parameters. Careful evaluation of clinical symptoms and thorough investigation of radiologic evidence of LRV compression is advisable before recommending surgical/endovascular intervention to obtain the best long-term outcomes. Patients with severe, classic, and chronic symptoms should be offered intervention. Renal vein transposition is safe and effective, and should be considered first-line therapy along with whatever adjuncts, including hybrid repair, needed to ensure a wide, tension-free anastomosis to the IVC. Early results of primary stenting are satisfactory, but long-term outcome results are limited. Both treatment modalities are invaluable in the event of failure of the other modality.
REFERENCES 1. Grant JCB, ed. A method of anatomy, descriptive and deductive. 3rd ed. Baltimore: The Williams and Wilkins company; 1944:822. xxiv. 2. Chait AMK, Fabian CE, Mellins HZ. Vascular impressions on the ureters. Am J Roentgen Rad Ther. 1971;3:729–749. 3. Stavros AT, Sickler KJ, Menter RR. Color duplex sonography of the nutcracker syndrome (aortomesenteric left renal vein compression). J Ultrasound Med. 1994;13(7):569–574. 4. Imamura A, Nakamura M, Maekawa N, et al. [Usefulness of renal CT scan for analysis of nutcracker phenomenon]. Nippon Hinyokika Gakkai Zasshi. 1992;83(11):1861–1865. 5. Wolfish NM, McLaine PN, Martin D. Renal vein entrapment syndrome: frequency and diagnosis—a lesson in conservatism. Clin Nephrol. 1986;26:96–100. 6. Arima MH, Hosokawa S, Ogino T. Ultrasonographically demonstrated nutcraker phenomenon: alternative to angiography. Int Urol Nephrol. 1990;22:3. 7. Takebayashi S, Ueki T, Ikeda N, et al. Diagnosis of the nutcracker syndrome with color Doppler sonography: correlation with flow patterns on retrograde left renal venography. AJR Am J Roentgenol. 1999;172(1):39–43. 8. Park SJ, Lim JW, Cho BS, et al. Nutcracker syndrome in children with orthostatic proteinuria: diagnosis on the basis of Doppler sonography. J Ultrasound Med. 2002;21(1):39–45, quiz 6. 9. Kim SH, Cho SW, Kim HD, et al. Nutcracker syndrome: diagnosis with Doppler US. Radiology. 1996;198(1):93–97. 10. Said SM, Gloviczki P, Kalra M, et al. Renal nutcracker syndrome: surgical options. Semin Vasc Surg. 2013;26(1):35–42. 11. Barnes RW, Fleisher HL 3rd, Redman JF, et al. Mesoaortic compression of the left renal vein (the so-called nutcracker syndrome): repair by a new stenting procedure. J Vasc Surg. 1988;8(4):415–421. 12. Reed NR, Kalra M, Bower TC, et al. Left renal vein transposition for nutcracker syndrome. J Vasc Surg. 2009;49(2):386–393, discussion 93–94. 13. Erben Y, Gloviczki P, Kalra M, et al. Treatment of nutcracker syndrome with open and endovascular interventions. J Vasc Surg Venous Lymphat Disord. 2015;3(4):389–396. 14. Ariyoshi A, Nagase K. Renal hematuria caused by “nutcracker” phenomenon: a more logical surgical management. Urology. 1990;35(2):168–170. 15. Wendel R, Crawford ED, Hehman K. The “nutcracker” phenomenon: an unusual cause for renal varicosities with hematuria. J Urol. 1980;123:761–763. 16. Lopatkin NA, Morozov AV, Lopatkina LN. Essential renal hemorrhages. Eur Urol. 1978;4:115–119.
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17. Zhang H, Zhang N, Li M, et al. Treatment of six cases of left renal nutcracker phenomenon: surgery and endografting. Chin Med J. 2003;116(11):1782–1784. 18. Scultetus AH, Villavicencio JL, Gillespie DL. The nutcracker syndrome: its role in the pelvic venous disorders. J Vasc Surg. 2001;34(5):812–819. 19. Lin WQ, Huang HF, Li M, et al. [Diagnosis and therapy of the nutcracker phenomenon: longterm follow-up]. Zhonghua Wai Ke Za Zhi. 2003;41(12):889–892. 20. Segawa N, Azuma H, Iwamoto Y, et al. Expandable metallic stent placement for nutcracker phenomenon. Urology. 1999;53(3):631–633. 21. Park YB, Lim SH, Ahn JH, et al. Nutcracker syndrome: intravascular stenting approach. Nephrol Dial Transplant. 2000;15(1):99–101. 22. Neste MG, Narasimham DL, Belcher KK. Endovascular stent placement as a treatment for renal venous hypertension. J Vasc Interv Radiol. 1996;7(6):859–861. 23. Kim SJ, Kim CW, Kim S, et al. Long-term follow-up after endovascular stent placement for treatment of nutcracker syndrome. J Vasc Interv Radiol. 2005;16(3):428–431. 24. Hartung O, Grisoli D, Boufi M, et al. Endovascular stenting in the treatment of pelvic vein congestion caused by nutcracker syndrome: lessons learned from the first five cases. J Vasc Surg. 2005;42(2):275–280. 25. Zhang H, Li M, Jin W, et al. The left renal entrapment syndrome: diagnosis and treatment. Ann Vasc Surg. 2007;21(2):198–203.