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Percutaneous Cryoablation of the Horseshoe Kidney: An Initial Experience
BRIEF REPORT
Percutaneous Cryoablation of the Horseshoe Kidney: An Initial Experience Junjian Huang, MD, Thomas D. Atwell, MD, A. Nicholas Kurup, MD, Stephen A. Boorjian, MD, R. Houston Thompson, MD, and Grant D. Schmit, MD ABSTRACT Between June 2006 and January 2016, 6 renal cryoablation procedures were performed in 5 patients with horseshoe kidneys. Renal cell carcinoma (RCC) accounted for 5 of the tumors, and the sixth was a carcinoid tumor. All 6 procedures were technically successful. The patient with the carcinoid tumor developed local tumor progression 38 months after ablation. Technique effectiveness was achieved in all 5 patients with RCC. Two complications occurred: obstructive hematuria and transient inguinal neuralgia after ablation. In this small initial experience, percutaneous cryoablation appears feasible in treatment of primary tumors in horseshoe kidneys.
ABBREVIATIONS eGFR = estimated glomerular filtration rate, RCC = renal cell carcinoma
Horseshoe kidney is the most common renal fusion anomaly and affects nearly 0.25% of live births (1). A horseshoe kidney develops during early organogenesis and is due to the fusion of the inferior poles, through either mechanical fusion or teratogenic migration of nephrogenic cells. The kidneys are joined by an isthmus that curtails the normal ascent of the kidneys owing to the presence of the inferior mesenteric artery; instead, the horseshoe kidney situates itself within the lower abdomen (1). The incidence of renal cell carcinoma (RCC) in patients with a horseshoe kidney is generally regarded as similar to the incidence in patients without the horseshoe variant (2). Horseshoe kidneys are at increased risk of otherwise rare renal masses, in particular, Wilms and carcinoid tumors with 4-fold and 62-fold relative risk, respectively (3,4). The accepted standard of treatment for these renal masses is surgical resection; however, the From the Department of Radiology (J.H.), Pennsylvania Hospital, Philadelphia, Pennsylvania; and Departments of Radiology (T.D.A., A.N.K., G.D.S.) and Urology (S.A.B., R.H.T.), Mayo Clinic, 200 First Street SW, Rochester, MN 55902. Received May 4, 2016; final revision received and accepted October 26, 2016. Address correspondence to T.D.A.; E-mail: atwell.thomas@mayo. edu None of the authors have identified a conflict of interest. & SIR, 2016 J Vasc Interv Radiol 2017; 28:498–501 http://dx.doi.org/10.1016/j.jvir.2016.10.026
procedure is technically challenging and associated with increased complications (5). More recently, alternative therapies such as percutaneous cryoablation have proven to be relatively safe and have achieved general acceptance in the treatment of small renal masses in select patients (6). Reports on ablative procedures in horseshoe kidneys are scarce in the literature. We present our initial experience using percutaneous cryoablation to treat tumors in this unique patient population.
MATERIALS AND METHODS Approval for this retrospective study was obtained from the institutional review board, and the study was compliant with the Health Insurance Portability and Accountability Act.
Sample Characteristics Data related to percutaneous image-guided cryoablation in horseshoe kidneys were collected prospectively in an institutional review board–approved tumor ablation treatment registry. Between June 2006 and January 2016, 5 patients with horseshoe kidneys containing 6 tumors were treated with 6 percutaneous renal ablation procedures (Table). The median age of patients at the time of the procedure was 65 years (range, 25–79 y). Most procedures were performed on male patients (83%). Following discussion of treatment options with a urologist with expertise in renal mass management,
No
2017
patients were referred to a radiologist to determine feasibility of ablation. With the exception of the ablative treatment, all patients were managed by the primary urologist. Median patient American Society of Anesthesiologists score was 2 (range, 1–2). Median estimated glomerular filtration rate (eGFR) for patients before treatment was 63 mL/min/1.73 m2 (range, 45–103 mL/ min/1.73 m2).
6 ASA ¼ American Society of Anesthesiologists; RCC ¼ renal cell carcinoma.
27
Grade 1/4 clear cell RCC
Yes
Grade 2/4 clear cell RCC
4.5 79 5
2
66 4
2
2.0
Yes
58 3 Grade 1/4 clear cell RCC Grade 2/4 clear cell RCC 64 68 3 3
2 2
3.7 2.5
Yes Yes
38 Yes Carcinoid 1.8 25 2
1
Biopsy
Grade 2/4 clear cell RCC 3.2
ASA Score
2 63 1
Age (y)
499
No
No No
No
Yes
’
Technical Features
73
Duration Imaging Follow-up
April
Maximum Tumor Size (cm)
Technical Success
’
Yes
Local Tumor Progression
Number 4
Patient
’
Table . Patient and Tumor Features and Outcomes
Volume 28
The procedure techniques have been previously described (7). Before ablation, screening for coagulopathy was performed to ensure a serum platelet count of Z 50 109/L and international normalized ratio of r 1.5. Antiplatelet agents such as aspirin and clopidogrel were withheld for at least 5 days before intervention. Cryoablation was performed under general anesthesia. Ultrasound and computed tomography (CT) guidance were used in combination on every case to accurately guide cryoprobes into the index tumor. An 18-gauge core biopsy device was used to obtain 1 or 2 samples from the mass immediately before treatment. The Endocare cryoablation system (Endocare, Inc, Irvine, California) was used in all cryoablation treatments. The number and size of probes used were based on tumor size, location, and anticipated ice ball geometry. A minimum of 2 probes were used per treatment, with an additional probe for each 1 cm of tumor size over 2 cm. Larger (2.4-mm outer diameter) cryoprobes were used to treat larger tumors (because of greater ice formation) and more central tumors (to better overcome thermal sink effects). Given the central location of the horseshoe kidney, hydrodisplacement was used in 3 patients to displace bowel. Care was taken to identify the ureter and avoid associated thermal injury (via CT monitoring). The tumors were treated using a conventional double freeze cycle using the argon-based cryosystem, with the duration of freeze determined by ice ball coverage of the tumor based on CT monitoring. The freeze cycles were separated by a 5-minute passive thaw. After the second freeze, the cryoprobes were actively warmed using helium and removed. Patients were admitted to the urology service after the procedure for overnight observation.
Data Collection Procedural complications were prospectively detailed and documented. The revised Clavien-Dindo classification system was used to grade complications for consistency with prior reports (8). Incidental, asymptomatic hematomas on CT and asymptomatic hematuria not requiring intervention were not considered complications, as these are frequently seen after percutaneous renal intervention (9,10). Patients were not routinely catheterized while under anesthesia, and transient, nonobstructive urine retention after ablation was considered within the normal clinical course. Technical success was
500
’
Percutaneous Cryoablation of Horseshoe Kidneys
defined as treatment of the index renal mass, and technique effectiveness was defined as complete ablation over the duration of follow-up (11). Local tumor progression was defined as new tumor in the ablation bed following technically successful treatment.
RESULTS All 6 procedures were technically successful. Of the 6 tumors, 5 (83%) were biopsy-proven RCC, with median size of 3.2 cm (range, 2.0–4.5 cm). A 25-year-old patient with prior partial nephrectomy for renal carcinoid tumor was found at biopsy to have recurrent carcinoid measuring 1.8 cm (Fig a–c). Stent placement and hydrodisplacement were used before the procedure in 1 of 6 and 3 of 6 procedures, respectively, to minimize risk of ureteral and bowel injury (12). Four patients were discharged the next day after routine overnight observation. One patient was hospitalized for 4 nights because of obstructive hematuria. Follow-up was maintained in all patients. Median imaging follow-up time was 33 months (range, 3–73 months). Technique effectiveness was demonstrated in all 5 patients treated for RCC, without local tumor progression at median 27 months (range, 3–73 months). One patient developed a second de novo RCC in the horseshoe kidney, remote in location from the initial index tumor, 4.5 years following ablation; this was also successfully treated with cryoablation. The patient treated for recurrent carcinoid in the horseshoe kidney (following prior partial nephrectomy) developed local tumor progression at 38 months after ablation; this patient is undergoing systemic treatment. Two patients have died. One patient died 24 months after ablation of unknown causes but without evidence of recurrent RCC during follow-up, and 1 patient died 46 months after ablation of chronic liver disease. At median follow-up of 33 months (range, 3–73 months),
Huang et al
’
JVIR
patients had a median change of eGFR of 2 mL/min/ 1.73 m2 (range, 36 to 22 mL/min/1.73 m2). There were 2 complications associated with the 6 ablation procedures. One patient experienced a transient decrease in eGFR from 51 mL/min/1.73 m2 before ablation to 10 mL/min/1.73 m2 2 days after ablation, which was related to obstructive hematuria; this patient’s renal function returned to baseline 2 days after ureteral stent placement (grade 3 complication). The second patient experienced transient neuralgia in the right inguinal region after ablation, which resolved by the 3-month follow-up visit (grade 1 complication). This neuralgia was likely due to the proximity of the ablation zone to the anterior right psoas muscle and genitofemoral nerve.
DISCUSSION There are approximately 200 reported cases of renal masses occurring within horseshoe kidneys in the Englishlanguage medical literature. This includes approximately 25 cases that were treated with surgical resection with variable success and relatively high complication rates (5). Surgery is technically challenging because of the lower anatomic position of the kidney, altered renal anatomy, and volatility of its vascular configuration. With its ascension blocked by the inferior mesenteric artery, a horseshoe kidney resides within the lower abdomen, malrotated and with its associated structures in variable configurations (1,5). The primary vascular tributaries to the horseshoe kidney are highly variable. Less than one third of horseshoe kidneys exhibit a single main renal artery, with a range of up to 8 renal arteries supplying each moiety. The minimally invasive surgical literature demonstrates increased blood loss, operative time, complications, and length of hospitalization for patients with horseshoe kidneys (5). With percutaneous cryoablation, such anatomic challenges can be navigated
Figure. A 25-year-old man with a carcinoid tumor in a horseshoe kidney. (a) T1-weighted magnetic resonance imaging with intravenous gadolinium contrast shows a 1.8-cm hypoenhancing mass (arrow) in the left moiety of the horseshoe kidney adjacent to the isthmus. (b) CT image obtained during cryoablation using 2 2.4-mm outer diameter cryoprobes shows a hypoattenuating ice ball (arrowheads) encompassing the mass. (c) CT image with intravenous contrast material obtained 24 months after ablation shows an involuted ablation defect with no residual tumor.
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Number 4
’
April
’
2017
through the use of real-time imaging and adjunctive maneuvers (11). Under ultrasound and CT guidance, the operator can minimize risk to adjacent vessels and viscera by using displacement techniques and varying the approach to placement of the individual ablation probes. A single case of radiofrequency ablation in a horseshoe kidney has been reported; however, cryoablation allows monitoring of the ablation zone with CT (13), which is of particular importance when treating an organ located centrally in the abdomen. Major complications following renal cryoablation are generally infrequent and include transient obstructive hematuria (2.6%) and bleeding/anemia (4.8%), with 40% of affected patients requiring transfusion and 55% requiring angiography and embolization (14). The results presented in the current series suggest that percutaneous cryoablation of tumors in horseshoe kidneys is feasible and has an acceptable complication profile. The dominant limitation of this study is its small sample size. Additionally, retrospective collection of some data is vulnerable to omissions in the medical record.
REFERENCES 1. Bauer SB. Anomalies of the upper urinary tract. In: Walsh PC, Retik AB, Vaughan ED, Wein AJ, eds. Campbell’s Urology, 8th ed. Philadelphia, PA: Saunders; 2002.
501
2. Stimac G, Dimanovski J, Ruzic B, et al. Tumours in kidney fusion anomalies—report of 5 cases and review of the literature. Scand J Urol Nephrol 2004; 38:485–489. 3. Mesrobian HG, Kelalis PP, Hrabovsky E, et al. Wilms’ tumor in horseshoe kidneys: a report from the National Wilms’ Tumor Study. J Urol 1985; 133:1002–1003. 4. Krishnan B, Truong LD, Saleh G, et al. Horseshoe kidney is associated with an increased relative risk of primary renal carcinoid tumor. J Urol 1997; 157:2059–2066. 5. Khan A, Myatt A, Palit V, et al. Laparoscopic heminephrectomy of a horseshoe kidney. JSLS 2011; 15:415–420. 6. Thompson RH, Atwell TD, Schmit GD, et al. Comparison of partial nephrectomy and percutaneous ablation for cT1 renal masses. Eur Urol 2015; 67:252–259. 7. Atwell TD, Callstrom MR, Schmit GD, et al. Percutaneous renal cryoablation: local control at mean 26 months of follow-up. J Urol 2010; 184:1291–1295. 8. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6,336 patients and results of a survey. Ann Surg 2004; 240:205–213. 9. Korbet SM. Percutaneous renal biopsy. Semin Nephrol 2002; 22: 254–267. 10. Ralls PW, Barakos JA, Kaptein EM, et al. Renal biopsy-related hemorrhage: frequency and comparison of CT and sonography. J Comput Assist Tomogr 1987; 11:1031–1034. 11. Ahmed M, Solbiati L, Brace CL, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. J Vasc Interv Radiol 2014; 25:1691–1705. 12. Bodily KD, Atwell TD, Mandrekar JN, et al. Hydrodisplacement in the percutaneous cryoablation of 50 renal tumors. AJR Am J Roentgenol 2010; 194:779–783. 13. Husillos-Alonso A, Bueno-Chomón G, Lledó-García E, et al. First percutaneous computed tomography-guided radiofrequency ablation of renal tumor in horseshoe kidney. Urology 2011; 78:466–468. 14. Atwell TD, Carter RE, Schmit GD, et al. Complications following 573 percutaneous renal radiofrequency and cryoablation procedures. J Vasc Interv Radiol 2012; 23:48–54.
Percutaneous Cryoablation of the Horseshoe Kidney: An Initial Experience Junjian Huang, MD, Thomas D. Atwell, MD, A. Nicholas Kurup, MD, Stephen A. Boorjian, MD, R. Houston Thompson, MD, and Grant D. Schmit, MD ABSTRACT Between June 2006 and January 2016, 6 renal cryoablation procedures were performed in 5 patients with horseshoe kidneys. Renal cell carcinoma (RCC) accounted for 5 of the tumors, and the sixth was a carcinoid tumor. All 6 procedures were technically successful. The patient with the carcinoid tumor developed local tumor progression 38 months after ablation. Technique effectiveness was achieved in all 5 patients with RCC. Two complications occurred: obstructive hematuria and transient inguinal neuralgia after ablation. In this small initial experience, percutaneous cryoablation appears feasible in treatment of primary tumors in horseshoe kidneys.
ABBREVIATIONS eGFR = estimated glomerular filtration rate, RCC = renal cell carcinoma
Horseshoe kidney is the most common renal fusion anomaly and affects nearly 0.25% of live births (1). A horseshoe kidney develops during early organogenesis and is due to the fusion of the inferior poles, through either mechanical fusion or teratogenic migration of nephrogenic cells. The kidneys are joined by an isthmus that curtails the normal ascent of the kidneys owing to the presence of the inferior mesenteric artery; instead, the horseshoe kidney situates itself within the lower abdomen (1). The incidence of renal cell carcinoma (RCC) in patients with a horseshoe kidney is generally regarded as similar to the incidence in patients without the horseshoe variant (2). Horseshoe kidneys are at increased risk of otherwise rare renal masses, in particular, Wilms and carcinoid tumors with 4-fold and 62-fold relative risk, respectively (3,4). The accepted standard of treatment for these renal masses is surgical resection; however, the From the Department of Radiology (J.H.), Pennsylvania Hospital, Philadelphia, Pennsylvania; and Departments of Radiology (T.D.A., A.N.K., G.D.S.) and Urology (S.A.B., R.H.T.), Mayo Clinic, 200 First Street SW, Rochester, MN 55902. Received May 4, 2016; final revision received and accepted October 26, 2016. Address correspondence to T.D.A.; E-mail: atwell.thomas@mayo. edu None of the authors have identified a conflict of interest. & SIR, 2016 J Vasc Interv Radiol 2017; 28:498–501 http://dx.doi.org/10.1016/j.jvir.2016.10.026
procedure is technically challenging and associated with increased complications (5). More recently, alternative therapies such as percutaneous cryoablation have proven to be relatively safe and have achieved general acceptance in the treatment of small renal masses in select patients (6). Reports on ablative procedures in horseshoe kidneys are scarce in the literature. We present our initial experience using percutaneous cryoablation to treat tumors in this unique patient population.
MATERIALS AND METHODS Approval for this retrospective study was obtained from the institutional review board, and the study was compliant with the Health Insurance Portability and Accountability Act.
Sample Characteristics Data related to percutaneous image-guided cryoablation in horseshoe kidneys were collected prospectively in an institutional review board–approved tumor ablation treatment registry. Between June 2006 and January 2016, 5 patients with horseshoe kidneys containing 6 tumors were treated with 6 percutaneous renal ablation procedures (Table). The median age of patients at the time of the procedure was 65 years (range, 25–79 y). Most procedures were performed on male patients (83%). Following discussion of treatment options with a urologist with expertise in renal mass management,
No
2017
patients were referred to a radiologist to determine feasibility of ablation. With the exception of the ablative treatment, all patients were managed by the primary urologist. Median patient American Society of Anesthesiologists score was 2 (range, 1–2). Median estimated glomerular filtration rate (eGFR) for patients before treatment was 63 mL/min/1.73 m2 (range, 45–103 mL/ min/1.73 m2).
6 ASA ¼ American Society of Anesthesiologists; RCC ¼ renal cell carcinoma.
27
Grade 1/4 clear cell RCC
Yes
Grade 2/4 clear cell RCC
4.5 79 5
2
66 4
2
2.0
Yes
58 3 Grade 1/4 clear cell RCC Grade 2/4 clear cell RCC 64 68 3 3
2 2
3.7 2.5
Yes Yes
38 Yes Carcinoid 1.8 25 2
1
Biopsy
Grade 2/4 clear cell RCC 3.2
ASA Score
2 63 1
Age (y)
499
No
No No
No
Yes
’
Technical Features
73
Duration Imaging Follow-up
April
Maximum Tumor Size (cm)
Technical Success
’
Yes
Local Tumor Progression
Number 4
Patient
’
Table . Patient and Tumor Features and Outcomes
Volume 28
The procedure techniques have been previously described (7). Before ablation, screening for coagulopathy was performed to ensure a serum platelet count of Z 50 109/L and international normalized ratio of r 1.5. Antiplatelet agents such as aspirin and clopidogrel were withheld for at least 5 days before intervention. Cryoablation was performed under general anesthesia. Ultrasound and computed tomography (CT) guidance were used in combination on every case to accurately guide cryoprobes into the index tumor. An 18-gauge core biopsy device was used to obtain 1 or 2 samples from the mass immediately before treatment. The Endocare cryoablation system (Endocare, Inc, Irvine, California) was used in all cryoablation treatments. The number and size of probes used were based on tumor size, location, and anticipated ice ball geometry. A minimum of 2 probes were used per treatment, with an additional probe for each 1 cm of tumor size over 2 cm. Larger (2.4-mm outer diameter) cryoprobes were used to treat larger tumors (because of greater ice formation) and more central tumors (to better overcome thermal sink effects). Given the central location of the horseshoe kidney, hydrodisplacement was used in 3 patients to displace bowel. Care was taken to identify the ureter and avoid associated thermal injury (via CT monitoring). The tumors were treated using a conventional double freeze cycle using the argon-based cryosystem, with the duration of freeze determined by ice ball coverage of the tumor based on CT monitoring. The freeze cycles were separated by a 5-minute passive thaw. After the second freeze, the cryoprobes were actively warmed using helium and removed. Patients were admitted to the urology service after the procedure for overnight observation.
Data Collection Procedural complications were prospectively detailed and documented. The revised Clavien-Dindo classification system was used to grade complications for consistency with prior reports (8). Incidental, asymptomatic hematomas on CT and asymptomatic hematuria not requiring intervention were not considered complications, as these are frequently seen after percutaneous renal intervention (9,10). Patients were not routinely catheterized while under anesthesia, and transient, nonobstructive urine retention after ablation was considered within the normal clinical course. Technical success was
500
’
Percutaneous Cryoablation of Horseshoe Kidneys
defined as treatment of the index renal mass, and technique effectiveness was defined as complete ablation over the duration of follow-up (11). Local tumor progression was defined as new tumor in the ablation bed following technically successful treatment.
RESULTS All 6 procedures were technically successful. Of the 6 tumors, 5 (83%) were biopsy-proven RCC, with median size of 3.2 cm (range, 2.0–4.5 cm). A 25-year-old patient with prior partial nephrectomy for renal carcinoid tumor was found at biopsy to have recurrent carcinoid measuring 1.8 cm (Fig a–c). Stent placement and hydrodisplacement were used before the procedure in 1 of 6 and 3 of 6 procedures, respectively, to minimize risk of ureteral and bowel injury (12). Four patients were discharged the next day after routine overnight observation. One patient was hospitalized for 4 nights because of obstructive hematuria. Follow-up was maintained in all patients. Median imaging follow-up time was 33 months (range, 3–73 months). Technique effectiveness was demonstrated in all 5 patients treated for RCC, without local tumor progression at median 27 months (range, 3–73 months). One patient developed a second de novo RCC in the horseshoe kidney, remote in location from the initial index tumor, 4.5 years following ablation; this was also successfully treated with cryoablation. The patient treated for recurrent carcinoid in the horseshoe kidney (following prior partial nephrectomy) developed local tumor progression at 38 months after ablation; this patient is undergoing systemic treatment. Two patients have died. One patient died 24 months after ablation of unknown causes but without evidence of recurrent RCC during follow-up, and 1 patient died 46 months after ablation of chronic liver disease. At median follow-up of 33 months (range, 3–73 months),
Huang et al
’
JVIR
patients had a median change of eGFR of 2 mL/min/ 1.73 m2 (range, 36 to 22 mL/min/1.73 m2). There were 2 complications associated with the 6 ablation procedures. One patient experienced a transient decrease in eGFR from 51 mL/min/1.73 m2 before ablation to 10 mL/min/1.73 m2 2 days after ablation, which was related to obstructive hematuria; this patient’s renal function returned to baseline 2 days after ureteral stent placement (grade 3 complication). The second patient experienced transient neuralgia in the right inguinal region after ablation, which resolved by the 3-month follow-up visit (grade 1 complication). This neuralgia was likely due to the proximity of the ablation zone to the anterior right psoas muscle and genitofemoral nerve.
DISCUSSION There are approximately 200 reported cases of renal masses occurring within horseshoe kidneys in the Englishlanguage medical literature. This includes approximately 25 cases that were treated with surgical resection with variable success and relatively high complication rates (5). Surgery is technically challenging because of the lower anatomic position of the kidney, altered renal anatomy, and volatility of its vascular configuration. With its ascension blocked by the inferior mesenteric artery, a horseshoe kidney resides within the lower abdomen, malrotated and with its associated structures in variable configurations (1,5). The primary vascular tributaries to the horseshoe kidney are highly variable. Less than one third of horseshoe kidneys exhibit a single main renal artery, with a range of up to 8 renal arteries supplying each moiety. The minimally invasive surgical literature demonstrates increased blood loss, operative time, complications, and length of hospitalization for patients with horseshoe kidneys (5). With percutaneous cryoablation, such anatomic challenges can be navigated
Figure. A 25-year-old man with a carcinoid tumor in a horseshoe kidney. (a) T1-weighted magnetic resonance imaging with intravenous gadolinium contrast shows a 1.8-cm hypoenhancing mass (arrow) in the left moiety of the horseshoe kidney adjacent to the isthmus. (b) CT image obtained during cryoablation using 2 2.4-mm outer diameter cryoprobes shows a hypoattenuating ice ball (arrowheads) encompassing the mass. (c) CT image with intravenous contrast material obtained 24 months after ablation shows an involuted ablation defect with no residual tumor.
Volume 28
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Number 4
’
April
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2017
through the use of real-time imaging and adjunctive maneuvers (11). Under ultrasound and CT guidance, the operator can minimize risk to adjacent vessels and viscera by using displacement techniques and varying the approach to placement of the individual ablation probes. A single case of radiofrequency ablation in a horseshoe kidney has been reported; however, cryoablation allows monitoring of the ablation zone with CT (13), which is of particular importance when treating an organ located centrally in the abdomen. Major complications following renal cryoablation are generally infrequent and include transient obstructive hematuria (2.6%) and bleeding/anemia (4.8%), with 40% of affected patients requiring transfusion and 55% requiring angiography and embolization (14). The results presented in the current series suggest that percutaneous cryoablation of tumors in horseshoe kidneys is feasible and has an acceptable complication profile. The dominant limitation of this study is its small sample size. Additionally, retrospective collection of some data is vulnerable to omissions in the medical record.
REFERENCES 1. Bauer SB. Anomalies of the upper urinary tract. In: Walsh PC, Retik AB, Vaughan ED, Wein AJ, eds. Campbell’s Urology, 8th ed. Philadelphia, PA: Saunders; 2002.
501
2. Stimac G, Dimanovski J, Ruzic B, et al. Tumours in kidney fusion anomalies—report of 5 cases and review of the literature. Scand J Urol Nephrol 2004; 38:485–489. 3. Mesrobian HG, Kelalis PP, Hrabovsky E, et al. Wilms’ tumor in horseshoe kidneys: a report from the National Wilms’ Tumor Study. J Urol 1985; 133:1002–1003. 4. Krishnan B, Truong LD, Saleh G, et al. Horseshoe kidney is associated with an increased relative risk of primary renal carcinoid tumor. J Urol 1997; 157:2059–2066. 5. Khan A, Myatt A, Palit V, et al. Laparoscopic heminephrectomy of a horseshoe kidney. JSLS 2011; 15:415–420. 6. Thompson RH, Atwell TD, Schmit GD, et al. Comparison of partial nephrectomy and percutaneous ablation for cT1 renal masses. Eur Urol 2015; 67:252–259. 7. Atwell TD, Callstrom MR, Schmit GD, et al. Percutaneous renal cryoablation: local control at mean 26 months of follow-up. J Urol 2010; 184:1291–1295. 8. Dindo D, Demartines N, Clavien PA. Classification of surgical complications: a new proposal with evaluation in a cohort of 6,336 patients and results of a survey. Ann Surg 2004; 240:205–213. 9. Korbet SM. Percutaneous renal biopsy. Semin Nephrol 2002; 22: 254–267. 10. Ralls PW, Barakos JA, Kaptein EM, et al. Renal biopsy-related hemorrhage: frequency and comparison of CT and sonography. J Comput Assist Tomogr 1987; 11:1031–1034. 11. Ahmed M, Solbiati L, Brace CL, et al. Image-guided tumor ablation: standardization of terminology and reporting criteria—a 10-year update. J Vasc Interv Radiol 2014; 25:1691–1705. 12. Bodily KD, Atwell TD, Mandrekar JN, et al. Hydrodisplacement in the percutaneous cryoablation of 50 renal tumors. AJR Am J Roentgenol 2010; 194:779–783. 13. Husillos-Alonso A, Bueno-Chomón G, Lledó-García E, et al. First percutaneous computed tomography-guided radiofrequency ablation of renal tumor in horseshoe kidney. Urology 2011; 78:466–468. 14. Atwell TD, Carter RE, Schmit GD, et al. Complications following 573 percutaneous renal radiofrequency and cryoablation procedures. J Vasc Interv Radiol 2012; 23:48–54.