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Evaluation of Color Doppler Intraoperative Ultrasound in Parenchymal Sparing Renal Surgery
0022-534 7/94/1526-1984$03. 00/0 Vol. 152, 1984-1987, December 1994 Printed in U.S.A.
THE JOURNAL OF UROLOGY
Copyright© 1994 by AMERICAN
UROLOGICAL AssOCIATION, INC.
EVALUATION OF COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING RENAL SURGERY McCLELLAN M. WALTHER, PETER L. CHOYKE, WENDOLIN HAYES, THOMAS H. SHAWKER, RICHARD B. ALEXANDER AND W. MARSTON LINEHAN From the Urologic Oncology Section, Surgery Branch, National Cancer Institute and Diagnostic Radiology Department, Warren G. Magnuson Clinical Center, National Institutes of Health, Bethesda, Maryland
ABSTRACT
A renal parenchymal sparing surgical approach may be recommended in select patients with von Hippel-Lindau disease and renal cancer or in those with _sporadic renal _canc~r and li11:1ited normal renal function. We performed 27 partial nephrectomies or enucleat10ns m 17 patients with the use of intraoperative ultrasound to examine a subset of all renal lesions identified on preoperative examination. . . . . . Of 24 lesions deep in the renal parenchyma that were exammed, localized or identified with intraoperative ultrasound 18 were characterized as cystic and 6 as solid. The deep cystic lesions were characterized with ultrasound as benign simple cysts. lntraoperative ultrasound was used to locate and mark the line of incision over 2 impalpable solid renal cell carcinomas. Four solid renal cell tumors extended deep into the renal parenchyma where color Doppler intraoperative ultrasound helped to define the plane of dissection adjacent to vital vascular structures. Renal hypothermia was not used in 3 renal operations based on intraoperative ultrasound findings. KEY WORDS:
kidney neoplasms, ultrasonography, Rippel-Lindau disease, nephrectomy
Intraoperative ultrasound has previously been described as an aid to parenchymal sparing surgery for sporadic renal tumors, 1 - 3 and in the evaluation of renal carcinoma vena caval thrombus. 4 While intraoperative ultrasound is not always needed, there is a subset of renal lesions in which its use can be helpful. Patients with multiple or large infiltrative tumors in whom renal preservation is an issue may benefit from intraoperative ultrasound. We evaluated a number of patients with metastatic sporadic renal cancer for treatment with interleukin-2 based protocols 5 and with von HippelLindau disease as part of screening studies to identify the von Rippel-Lindau disease gene. 6 von Rippel-Lindau disease is an autosomal dominant condition characterized by retinal angiomas, central nervous system hemangioblastomas, pancreatic cysts and tumors, pheochromocytomas and multiple, often bilateral renal cysts, as well as cystic and solid renal tumors. 7 - 9 Renal tumors have been found in 24 to 55% of the patients with von HippelLindau disease, 7 • 9 - 11 and metastases from renal carcinoma account for approximately 13 to 42% of von Rippel-Lindau disease patient deaths. 7 - 9 A renal parenchymal sparing surgical approach with partial nephrectomy and enucleation has been useful in the treatment of select patients with von Rippel-Lindau disease and renal cancer. Patients with limited renal function and renal cancer have also derived benefit from parenchymal sparing operations. 12 Some renal tumors are deep in the cortex and are not visible or palpable to the surgeon, or they are in the renal hilus contiguous with vital vascular structures. Large renal lesions may have an infiltrative component whose margin is not well defined at surgical exploration. 13 Examination or localization of these structures in relation to the lesion of interest can be of great help to the surgeon. The parenchymal sparing techniques used in patients with von HippelLindau disease can be helpful in any patient when conservation of renal parenchyma is important. We investigated the use of intraoperative ultrasound in patients with sporadic and inherited forms of renal cancer. Accepted for publication May 13, 1994.
MATERIALS AND METHODS
Between May 1989 and January 1993, intraoperative ultrasound was performed in conjunction with 27 renal operations in 11 men and 6 women (16 white and 1 Hispanic) with renal tumors. Mean patient age was 39.8 years (range 20 to 57). Preoperative evaluation consisted of contrast enhanced computerized tomography (CT) and renal ultrasound in all cases. Renal arteriography was performed when clinically indicated. A total of 14 patients with von Rippel-Lindau disease underwent 23 renal operations, 1 with hereditary multifocal, papillary renal cell carcinoma was explored once and 2 with sporadic renal cell carcinoma underwent 3 renal explorations. All patients chose a renal parenchymal sparing operation. A total of 337 renal lesions was diagnosed and 319 were surgically removed (mean 12.3 lesions per kidney, range 1 to 29). Of the lesions 206 (62%) were identified on preoperative studies (including 2 false-positive readings), while 128 of 334 (38%) were identified by visual inspection of the kidney and excised by the surgeon. The majority of lesions not detected by CT were small surface cysts or tumors. Intraoperative color Doppler ultrasonography was performed by the surgeon using a Diasonics Spectra or Wide Vu machine. A 5 or 10 MHz. linear array transducer was placed in a sterile ultrasound sheath with sterile gel inside the sheath. Saline, warmed to near body temperature, was placed in the wound to act as a sonographic coupling agent. The kidney was mobilized and Gerota's fascia was opened so all surfaces could be evaluated. lntraoperative ultrasound was performed before any lesions were removed. Larger lesions, at risk for greater hemorrhage, were generally removed last. After smaller, more easily resectable lesions were removed, intraoperative ultrasound was performed to evaluate lesions of interest. A 5 MHz. transducer placed on the surface of the kidney was used most frequently, which allowed for good resolution of the kidney parenchyma and deep vital structures, such as vessels and collecting system. Surface lesions were examined most frequently with the 10 MHz. transducer and sometimes required scanning with the transducer placed 1 to 2 cm. above the surface of the kidney to remove transducer artifact. Scanning was performed in a
1984
COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING SURGERY
sequential fashion from upper to lower pole in the longitudinal and transverse planes, first on the anterior and then on the posterior surfaces of the kidney. The images were evaluated prospectively by the radiologist in attendance (P. L. C., W. H . and T. H . S.) and video recorded. Freeze frame images were obtained to assess tumor size, tumor characterization and depth of parenchymal extension. Color Doppler ultrasonography was used to evaluate the proximity of vessels, and the depth of each large lesion and its relationship to the collecting system were assessed with color and gray scale ultrasound. Hypothermia was induced after intraoperative ultrasound determined that adjacent vessels required occlusion to remove the lesion safely. RESULTS
Preoperative CT evaluation and intraoperative visual examination of the kidney identified most (334 of 338) renal lesions. One cystic renal cell carcinoma and 3 renal cysts were detected only by intraoperative ultrasound. The majority of renal lesions did not require ultrasound for localization or evaluation of adjacent structures. Intraoperative ultrasound was particularly useful in 24 of 338 renal lesions (7%, 18 cystic and 6 solid) that were deep to the cortical surface or extended deep into the renal hilum, causing problems in localization or planning the line of incision in the renal parenchyma. Of 24 renal lesions 20 (18 cystic and 2 solid) identified by preoperative CT could not be localized by the surgeon and were found only through the use of intraoperative ultrasound. The 18 cystic lesions were deep in the renal parenchyma, characterized with ultrasound as benign simple cysts and left in place. Two solid renal tumors deep in the renal parenchyma were not visible or palpable, and could only be localized by intraoperative ultrasound. Four solid lesions extended deep into the renal parenchyma, where color Doppler intraoperative ultrasound helped define the plane of dissection adjacent to vital vascular structures. No significant vascularity was demonstrated adjacent to 3 of 27 solid lesions (11 %, 2 von Rippel-Lindau disease and 1 sporadic), changing the operation to one without hypothermia. Before closure intraoperative ultrasound was often used to examine the kidney for residual lesions. We detected 1 missed cystic renal carcinoma in the last 6 renal operations when intraoperative ultrasound was routinely performed before closure. lntraoperative ultrasound was also done to stage and limit dissection around a renal vein thrombus that was not diagnosed on preoperative studies. The use of intraoperative ultrasound is demonstrated in 4 patients.
1985
CASE HISTORIES
Case 1. A 27-year-old white man was found to have multiple renal lesions after screening radiological studies of von Rippel-Lindau disease kindred (fig. 1, A). After discussing the alternatives of bilateral nephrectomy with dialysis or renal transplantation, watchful waiting and a parenchymal sparing operation, the patient chose the latter procedure. At renal exploration multiple renal lesions were identified. One solid lesion identified on CT could not be palpated after interruption of the renal vascular flow and renal cooling. Renal ultrasound identified the lesion and deep vascular structures adjacent to it. The ultrasound probe was used to mark the renal cortex nephrotomy incision made to remove the mass (fig. 1, B). Pathological examination revealed renal cell carcinoma with clear cell features. Case 2. A 62-year-old man with von Rippel-Lindau disease had right renal cysts and tumors 12 years after right partial nephrectomy for renal cell carcinoma. Superficial lesions were resected without renal hypothermia. The largest solid lesion was partially visible in the medial aspect of the lower pole of the kidney near the renal hilum (fig. 2, A). A small polar artery not identified by preoperative studies was seen by intraoperative ultrasound to enter the renal parenchyma directly over the renal cancer (fig. 2, B). Temporary occlusion of the polar artery demonstrated ischemic changes in less than 10% of the kidney. Significantly, the area of ischemia corresponded to the area overlying the renal mass localized by intraoperative ultrasound, and identified the line of incision in the renal cortex needed to remove the tumor with minimal blood loss after ligation of the polar artery. Pathological examination revealed a renal cell carcinoma of clear and granular cell type. In addition, 2 deep renal cysts not detected by preoperative CT were noted with intraoperative ultrasound. The cysts were simple in nature and left in place. Case 3. A 22-year-old white woman was found to have multiple renal lesions during screening radiological examinations of von Rippel-Lindau disease kindred (fig. 3, A). Exploration and parenchymal sparing surgery were done. A solid hilar mass immediately adjacent to the renal vein was identified by intraoperative ultrasound. The renal mass was visualized and a cystic lesion, not noted on preoperative CT, was found deep to the solid mass. Color Doppler study of the tumor showed the renal vein and artery below the lesion, with a rim of renal parenchyma adjacent to the renal vein (fig. 3, B). The tumor and cyst were circumscribed bluntly with a Penfield neurosurgical dissector without the need for renal hypothermia. Pathological examination revealed renal
FIG. 1. Case 1. A, deep parenchymal lesion in right kidney nonpalpable to surgeon, seen on preoperative CT. B, color Doppler ultrasound demonstrates deep solid mass (arrow) with prominent sinus vessels adjacent to lesion. Star marks surface of kidney.
1986
COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING SURGERY
FIG. 2. Case 2. A, preoperative CT shows solid hilar mass on right side (arrow) with 2 smaller cysts more laterally. B, color Doppler image demonstrates relationship of hilar mass (M) to deep hilar vessels (arrow) shown in color . Star marks surface of kidney.
FIG. 3. Case 3. A, preoperative CT reveals solid renal mass deep to surface of kidney (arrow). B , intraoperative ultrasound with color Doppler. With transducer compressing anterior surface of kidney (star), highly echogenic lesion is demonstrated just below posterior renal surface. Renal vasculature (arrow) is seen just deep to lesion.
cell carcinoma with spindle cell features. A simple cyst, not identified by preoperative studies, was also found in the upper pole of the kidney after all lesions had been excised. Intraoperative ultrasound was performed at the end of the procedure and no other renal lesions were noted. Case 4. A 57-year-old white man with von Rippel-Lindau disease had an enlarging right renal hilar mass 3 years after resection of several renal cell carcinomas from that kidney. At renal exploration a tumor thrombus, not appreciated on preoperative studies, was palpated in the renal vein. Dense fibrous tissue from the previous renal surgery did not allow for evaluation of tumor thrombus extension by palpation. Intraoperative ultrasound allowed for rapid assessment of the extent of the thrombus, minimizing dissection in a previously operated area.
DISCUSSION
lntraoperative ultrasound has found broad use in surgical procedures involving the brain, 14 pancreas 15• 16 and hepatobiliary tree.16 Renal intraoperative ultrasound was originally performed for stone disease, 1 7 and subsequently for the evaluation of renal cancer1--3 and vena caval thrombi.4 Recent technical advancements have included color Doppler ultrasound for demonstration of renal vasculature. We have found intraoperative ultrasound to be useful in patients undergoing parenchymal sparing procedures or who require intraoperative assessment of findings not diagnosed on preoperative studies. Renal parenchymal sparing surgery ideally removes clinically detectable cancer while retaining renal function. This approach is best suited for patients with multiple renal tu-
COLOR DOPPLEit II\fTF~ltOPEE~4.TP:/E OLTRASOU:ND ft\! PAR,El'lCHYlVIAL SPA_RING STJRGER:!
mors or solitary tumors with limited normal renal function.12· 13 We evaluated patients with von Hippel-Lindau disease as part of a strategy to identify the von Rippel-Lindau disease gene. 6 Bilateral renal carcinomas develop in 60 to 75% of patients with von Rippel-Lindau disease and renal lesions. 4 • 11 • 18 • 19 While these tumors can be of low grade if detected early through screening of affected kindreds, metastases from renal carcinoma represent a major cause of death in von Rippel-Lindau disease patients. 7 - 9 We have also seen patients with metastatic renal cancer undergo remission after interleukin-2 based treatments and subsequently have isolated renal metastases. 20 Intraoperative ultrasound was helpful in characterizing the multiple, bilateral tumors or solitary deep sporadic lesions present in these patient groups. Preoperative CT and operative visualization of the kidney identified most (332 of 338) renal lesions. We found intraoperative ultrasound useful in the examination, localization or removal of a small subset (7%) of renal lesions identified previously. Gray scale sonograms were used to characterize lesions that were indeterminate on preoperative studies and to localize lesions demonstrated by preoperative studies but not apparent in the operating room.2· 3 We used a 5 MHz. transducer to visualize deep renal lesions. Adequate coupling was achieved by filling the incision with water or saline. Transducer artifact was not a problem, since the region of interest was the deeper aspect of the renal tumors. A superficial lesion was examined by moving the transducer to an adjacent area or to the other side of the kidney. Solid renal lesions in the hilum or deep in the renal parenchyma were examined with intraoperative ultrasound to evaluate the margin of normal tissue, which defines the resection and any vital adjacent structures. Color Doppler ultrasound identified arteries, veins and the urinary collecting system near the potential resection site, and estimated the thickness of renal parenchymal margin between the tumor and vessel. In 3 operations (11%) intraoperative ultrasound determined that there were no immediately adjacent renal vessels and that a lesion could be removed without the need for renal hypothermia, sparing unnecessary renal hilar dissection. Intraoperative ultrasound was also used in 1 patient to evaluate a renal vein thrombus not identified on preoperative studies. The use of intraoperative ultrasound to identify a renal vein thrombus in patients with renal cell carcinoma has already been reported. 4 Our experience demonstrates the spectrum of use ofintraoperative ultrasound in select lesions as an aid to renal parenchymal sparing surgery in general and in patients with von Rippel-Lindau disease in particular, and in the evaluation of unexpected renal vein thrombus. Judicious use of intraoperative ultrasound on lesions that are more difficult to resect can alter the surgical technique and decrease blood loss. Intraoperative ultrasound can be performed to evaluate the margin of large infiltrative lesions, when the surgical margin is not always apparent and when there is known to be a risk of small satellite tumors. 13 • 21 In these patients an adequate margin can be described by intraoperative ultrasound and satellite lesions can be removed. The use of intraoperative ultrasound was complimentary to and further refined the data obtained by the preoperative evaluation. We found intraoperative ultrasound to be particularly helpful in characterizing deep parenchymal cystic lesions and evaluating larger deep or hilar solid tumors. In our hands, intraoperative ultrasound was a tool to minimize blood and renal parenchymal loss, allowing safe removal of a renal lesion and subsequent pathological diagnosis. We recommend a high frequency color Doppler transducer to provide greater anatomical resolution of the tumor, margin of resection and surrounding structures. Intraoperative ultrasound performed before closure in patients with many renal lesions ensures that the kidney is thoroughly inspected, thus maximizing the benefit from each operation.
1987
REFERENCES
L Assimos, D. G., Boyce, H., Woodruff, R. D., Harrison, L. H., McCullough, D. L. and Kroovand, R. L.: Intraoperative renal ultrasonography: a useful adjunct to partial nephrectomy. J. UroL, 146: 1218, 1991. 2. Gilbert, B. R., Russo, P., Zirinsky, K., Kazam, E., Fair, W.R. and Vaughan, E. D., Jr.:Intraoperative sonography: application in renal cell carcinoma. J. Urol., 139: 582, 1988.
3. Marshall, F. F., Holdford, S.S. and Hamper, U. M.: Intraoperative sonography of renal tumors. J. Urol., 148: 1393, 1992. 4. Long, J.P., Choyke, P. L., Shawker, T. A., Robertson, C. A., Pass, H. I., Walther, M. M. and Linehan, W. M.: Intraoperative ultrasound in the evaluation of tumor involvement of the inferior vena cava. J. UroL, 150: 13, 1993. 5. Walther, M. M., Alexander, R. B., Weiss, G. H., Venzon, D., Berman, A., Pass, H. I., Linehan, W. M. and Rosenberg, S. A.: Cytoreductive surgery prior to interleukin-2 based therapy in patients with metastatic renal cell carcinoma. Urology, 42: 250, 1993. 6. Latif, F., Tory, K., Gnarra, J., Yao, M., Duh, F. M., Orcutt, M. L., Stackhouse, T., Kuzmin, I., Modi, W., Geil, L. et al: Identification of the von Rippel-Lindau disease tumor suppressor gene. Science, 260: 1317, 1993. 7. Glenn, G., Choyke, P., Zbar, B. and Linehan, W. M.: von HippelLindau disease: clinical review and molecular genetics. Prob. Urol., 4: 312, 1990. 8. Horton, W. A., Wong, V. and Eldridge, R.: von Rippel-Lindau disease: clinical and pathological manifestations in nine families with 50 affected members. Arch. Intern. Med., 136: 769, 1976. 9. Lamiell, J.M., Salazar, F. G. and Hsia, Y. E.: von Rippel-Lindau disease affecting 43 members of a single kindred. Medicine, 68: 1, 1989. 10. Solomon, D. and Schwartz, A.: Renal pathology in von HippelLindau disease. Hum. Path., 19: 1072, 1988. 11. Poston, C. D., Jaffe, G. S., Lubensky, I. A., Linehan, W. M. and Walther, M. M.: Characterization of the renal pathology of a familial form of renal cell carcinoma associated with von Rippel-Lindau disease: clinical and molecular genetic implications. J. Urol., in press 12. Licht, M. R. and Novick, A C.: Nephron sparing surgery for renal cell carcinoma. J. Urol., 149: 1, 1992. 13. Marshall, F. F., Taxy, J.B., Fishman, E. K. and Chang, R.: The feasibility of surgical enucleation for renal cell carcinoma. J. Urol., 135: 231, 1986. 14. Avila, N. A, Shawker, T. H., Choyke, P. L. and Oldfield, E. H.: Cerebellar and spinal hemangioblastomas: evaluation with intraoperative gray-scale color Doppler flow US. Radiology, 188: 143, 1993. 15. Chern.er, J. A., Doppman, J. L., Norton, J. A., Miller, D. L., Krudy, A G., Raufman, J. P., Collen, M. J., Matan, P. N., Gardner, J. D. and Jensen, R. T.: Selective venous sampling for gastrin to localize gastrinornas. A prospective assessment. Ann. Intern. Med., 105: 841, 1986. 16. Machi, J., Sigel, B., Zaren, H. A., Kurohiji, T. and Yamashita, Y.: Operative ultrasonography during hepatobiliary and pancreatic surgery. World J. Surg., 17: 640, 1993. 17. Cook, J. H., HI and Lytton, B.: The practical use of ultrasound as an adjunct to renal calculous surgery. Urol. Clin. N. Amer., 8: 319, 1981. 18. Choyke, P. L., Glenn, G. M., Walther, M. M., Zbar, B., Weiss, G. H., Alexander, R. B., Hayes, W. 8., Long, J. P., Thakore, K. N. and Linehan, W. M.: The natural history of renal lesions in von Rippel-Lindau disease: a serial CT study in 28 patients. AJR, 159: 1229, 1992. 19. Choyke, P. L., Filling-Katz, M. R., Shawker, T. H., Gorin, M. B., Travis, W. D., Chang, R., Seizinger, B. R., Dwyer, A. J. and Linehan, W. M.: von Rippel-Lindau disease: radiologic screening for visceral manifestations. Radiology, 174: 815, 1990. 20. Long, J. P., Walther, M. M., Alexander, R. B., Linehan, W. M. and Rosenberg, S. A.: The management of isolated renal recurrence ofrenal cell carcinoma following complete response to interleukin-2 based immunotherapy. J. Urol., 150: 176, 1993. 21. Novick, A. C., Streem, 8., Montie, J. E., Pontes, J. E., Siegel, S., Montague, D. K. and Goormastic, M.: Conservative surgery for renal cell carcinoma: a single-center experience with 100 patients. J. Urol., 141: 835, 1989.
THE JOURNAL OF UROLOGY
Copyright© 1994 by AMERICAN
UROLOGICAL AssOCIATION, INC.
EVALUATION OF COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING RENAL SURGERY McCLELLAN M. WALTHER, PETER L. CHOYKE, WENDOLIN HAYES, THOMAS H. SHAWKER, RICHARD B. ALEXANDER AND W. MARSTON LINEHAN From the Urologic Oncology Section, Surgery Branch, National Cancer Institute and Diagnostic Radiology Department, Warren G. Magnuson Clinical Center, National Institutes of Health, Bethesda, Maryland
ABSTRACT
A renal parenchymal sparing surgical approach may be recommended in select patients with von Hippel-Lindau disease and renal cancer or in those with _sporadic renal _canc~r and li11:1ited normal renal function. We performed 27 partial nephrectomies or enucleat10ns m 17 patients with the use of intraoperative ultrasound to examine a subset of all renal lesions identified on preoperative examination. . . . . . Of 24 lesions deep in the renal parenchyma that were exammed, localized or identified with intraoperative ultrasound 18 were characterized as cystic and 6 as solid. The deep cystic lesions were characterized with ultrasound as benign simple cysts. lntraoperative ultrasound was used to locate and mark the line of incision over 2 impalpable solid renal cell carcinomas. Four solid renal cell tumors extended deep into the renal parenchyma where color Doppler intraoperative ultrasound helped to define the plane of dissection adjacent to vital vascular structures. Renal hypothermia was not used in 3 renal operations based on intraoperative ultrasound findings. KEY WORDS:
kidney neoplasms, ultrasonography, Rippel-Lindau disease, nephrectomy
Intraoperative ultrasound has previously been described as an aid to parenchymal sparing surgery for sporadic renal tumors, 1 - 3 and in the evaluation of renal carcinoma vena caval thrombus. 4 While intraoperative ultrasound is not always needed, there is a subset of renal lesions in which its use can be helpful. Patients with multiple or large infiltrative tumors in whom renal preservation is an issue may benefit from intraoperative ultrasound. We evaluated a number of patients with metastatic sporadic renal cancer for treatment with interleukin-2 based protocols 5 and with von HippelLindau disease as part of screening studies to identify the von Rippel-Lindau disease gene. 6 von Rippel-Lindau disease is an autosomal dominant condition characterized by retinal angiomas, central nervous system hemangioblastomas, pancreatic cysts and tumors, pheochromocytomas and multiple, often bilateral renal cysts, as well as cystic and solid renal tumors. 7 - 9 Renal tumors have been found in 24 to 55% of the patients with von HippelLindau disease, 7 • 9 - 11 and metastases from renal carcinoma account for approximately 13 to 42% of von Rippel-Lindau disease patient deaths. 7 - 9 A renal parenchymal sparing surgical approach with partial nephrectomy and enucleation has been useful in the treatment of select patients with von Rippel-Lindau disease and renal cancer. Patients with limited renal function and renal cancer have also derived benefit from parenchymal sparing operations. 12 Some renal tumors are deep in the cortex and are not visible or palpable to the surgeon, or they are in the renal hilus contiguous with vital vascular structures. Large renal lesions may have an infiltrative component whose margin is not well defined at surgical exploration. 13 Examination or localization of these structures in relation to the lesion of interest can be of great help to the surgeon. The parenchymal sparing techniques used in patients with von HippelLindau disease can be helpful in any patient when conservation of renal parenchyma is important. We investigated the use of intraoperative ultrasound in patients with sporadic and inherited forms of renal cancer. Accepted for publication May 13, 1994.
MATERIALS AND METHODS
Between May 1989 and January 1993, intraoperative ultrasound was performed in conjunction with 27 renal operations in 11 men and 6 women (16 white and 1 Hispanic) with renal tumors. Mean patient age was 39.8 years (range 20 to 57). Preoperative evaluation consisted of contrast enhanced computerized tomography (CT) and renal ultrasound in all cases. Renal arteriography was performed when clinically indicated. A total of 14 patients with von Rippel-Lindau disease underwent 23 renal operations, 1 with hereditary multifocal, papillary renal cell carcinoma was explored once and 2 with sporadic renal cell carcinoma underwent 3 renal explorations. All patients chose a renal parenchymal sparing operation. A total of 337 renal lesions was diagnosed and 319 were surgically removed (mean 12.3 lesions per kidney, range 1 to 29). Of the lesions 206 (62%) were identified on preoperative studies (including 2 false-positive readings), while 128 of 334 (38%) were identified by visual inspection of the kidney and excised by the surgeon. The majority of lesions not detected by CT were small surface cysts or tumors. Intraoperative color Doppler ultrasonography was performed by the surgeon using a Diasonics Spectra or Wide Vu machine. A 5 or 10 MHz. linear array transducer was placed in a sterile ultrasound sheath with sterile gel inside the sheath. Saline, warmed to near body temperature, was placed in the wound to act as a sonographic coupling agent. The kidney was mobilized and Gerota's fascia was opened so all surfaces could be evaluated. lntraoperative ultrasound was performed before any lesions were removed. Larger lesions, at risk for greater hemorrhage, were generally removed last. After smaller, more easily resectable lesions were removed, intraoperative ultrasound was performed to evaluate lesions of interest. A 5 MHz. transducer placed on the surface of the kidney was used most frequently, which allowed for good resolution of the kidney parenchyma and deep vital structures, such as vessels and collecting system. Surface lesions were examined most frequently with the 10 MHz. transducer and sometimes required scanning with the transducer placed 1 to 2 cm. above the surface of the kidney to remove transducer artifact. Scanning was performed in a
1984
COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING SURGERY
sequential fashion from upper to lower pole in the longitudinal and transverse planes, first on the anterior and then on the posterior surfaces of the kidney. The images were evaluated prospectively by the radiologist in attendance (P. L. C., W. H . and T. H . S.) and video recorded. Freeze frame images were obtained to assess tumor size, tumor characterization and depth of parenchymal extension. Color Doppler ultrasonography was used to evaluate the proximity of vessels, and the depth of each large lesion and its relationship to the collecting system were assessed with color and gray scale ultrasound. Hypothermia was induced after intraoperative ultrasound determined that adjacent vessels required occlusion to remove the lesion safely. RESULTS
Preoperative CT evaluation and intraoperative visual examination of the kidney identified most (334 of 338) renal lesions. One cystic renal cell carcinoma and 3 renal cysts were detected only by intraoperative ultrasound. The majority of renal lesions did not require ultrasound for localization or evaluation of adjacent structures. Intraoperative ultrasound was particularly useful in 24 of 338 renal lesions (7%, 18 cystic and 6 solid) that were deep to the cortical surface or extended deep into the renal hilum, causing problems in localization or planning the line of incision in the renal parenchyma. Of 24 renal lesions 20 (18 cystic and 2 solid) identified by preoperative CT could not be localized by the surgeon and were found only through the use of intraoperative ultrasound. The 18 cystic lesions were deep in the renal parenchyma, characterized with ultrasound as benign simple cysts and left in place. Two solid renal tumors deep in the renal parenchyma were not visible or palpable, and could only be localized by intraoperative ultrasound. Four solid lesions extended deep into the renal parenchyma, where color Doppler intraoperative ultrasound helped define the plane of dissection adjacent to vital vascular structures. No significant vascularity was demonstrated adjacent to 3 of 27 solid lesions (11 %, 2 von Rippel-Lindau disease and 1 sporadic), changing the operation to one without hypothermia. Before closure intraoperative ultrasound was often used to examine the kidney for residual lesions. We detected 1 missed cystic renal carcinoma in the last 6 renal operations when intraoperative ultrasound was routinely performed before closure. lntraoperative ultrasound was also done to stage and limit dissection around a renal vein thrombus that was not diagnosed on preoperative studies. The use of intraoperative ultrasound is demonstrated in 4 patients.
1985
CASE HISTORIES
Case 1. A 27-year-old white man was found to have multiple renal lesions after screening radiological studies of von Rippel-Lindau disease kindred (fig. 1, A). After discussing the alternatives of bilateral nephrectomy with dialysis or renal transplantation, watchful waiting and a parenchymal sparing operation, the patient chose the latter procedure. At renal exploration multiple renal lesions were identified. One solid lesion identified on CT could not be palpated after interruption of the renal vascular flow and renal cooling. Renal ultrasound identified the lesion and deep vascular structures adjacent to it. The ultrasound probe was used to mark the renal cortex nephrotomy incision made to remove the mass (fig. 1, B). Pathological examination revealed renal cell carcinoma with clear cell features. Case 2. A 62-year-old man with von Rippel-Lindau disease had right renal cysts and tumors 12 years after right partial nephrectomy for renal cell carcinoma. Superficial lesions were resected without renal hypothermia. The largest solid lesion was partially visible in the medial aspect of the lower pole of the kidney near the renal hilum (fig. 2, A). A small polar artery not identified by preoperative studies was seen by intraoperative ultrasound to enter the renal parenchyma directly over the renal cancer (fig. 2, B). Temporary occlusion of the polar artery demonstrated ischemic changes in less than 10% of the kidney. Significantly, the area of ischemia corresponded to the area overlying the renal mass localized by intraoperative ultrasound, and identified the line of incision in the renal cortex needed to remove the tumor with minimal blood loss after ligation of the polar artery. Pathological examination revealed a renal cell carcinoma of clear and granular cell type. In addition, 2 deep renal cysts not detected by preoperative CT were noted with intraoperative ultrasound. The cysts were simple in nature and left in place. Case 3. A 22-year-old white woman was found to have multiple renal lesions during screening radiological examinations of von Rippel-Lindau disease kindred (fig. 3, A). Exploration and parenchymal sparing surgery were done. A solid hilar mass immediately adjacent to the renal vein was identified by intraoperative ultrasound. The renal mass was visualized and a cystic lesion, not noted on preoperative CT, was found deep to the solid mass. Color Doppler study of the tumor showed the renal vein and artery below the lesion, with a rim of renal parenchyma adjacent to the renal vein (fig. 3, B). The tumor and cyst were circumscribed bluntly with a Penfield neurosurgical dissector without the need for renal hypothermia. Pathological examination revealed renal
FIG. 1. Case 1. A, deep parenchymal lesion in right kidney nonpalpable to surgeon, seen on preoperative CT. B, color Doppler ultrasound demonstrates deep solid mass (arrow) with prominent sinus vessels adjacent to lesion. Star marks surface of kidney.
1986
COLOR DOPPLER INTRAOPERATIVE ULTRASOUND IN PARENCHYMAL SPARING SURGERY
FIG. 2. Case 2. A, preoperative CT shows solid hilar mass on right side (arrow) with 2 smaller cysts more laterally. B, color Doppler image demonstrates relationship of hilar mass (M) to deep hilar vessels (arrow) shown in color . Star marks surface of kidney.
FIG. 3. Case 3. A, preoperative CT reveals solid renal mass deep to surface of kidney (arrow). B , intraoperative ultrasound with color Doppler. With transducer compressing anterior surface of kidney (star), highly echogenic lesion is demonstrated just below posterior renal surface. Renal vasculature (arrow) is seen just deep to lesion.
cell carcinoma with spindle cell features. A simple cyst, not identified by preoperative studies, was also found in the upper pole of the kidney after all lesions had been excised. Intraoperative ultrasound was performed at the end of the procedure and no other renal lesions were noted. Case 4. A 57-year-old white man with von Rippel-Lindau disease had an enlarging right renal hilar mass 3 years after resection of several renal cell carcinomas from that kidney. At renal exploration a tumor thrombus, not appreciated on preoperative studies, was palpated in the renal vein. Dense fibrous tissue from the previous renal surgery did not allow for evaluation of tumor thrombus extension by palpation. Intraoperative ultrasound allowed for rapid assessment of the extent of the thrombus, minimizing dissection in a previously operated area.
DISCUSSION
lntraoperative ultrasound has found broad use in surgical procedures involving the brain, 14 pancreas 15• 16 and hepatobiliary tree.16 Renal intraoperative ultrasound was originally performed for stone disease, 1 7 and subsequently for the evaluation of renal cancer1--3 and vena caval thrombi.4 Recent technical advancements have included color Doppler ultrasound for demonstration of renal vasculature. We have found intraoperative ultrasound to be useful in patients undergoing parenchymal sparing procedures or who require intraoperative assessment of findings not diagnosed on preoperative studies. Renal parenchymal sparing surgery ideally removes clinically detectable cancer while retaining renal function. This approach is best suited for patients with multiple renal tu-
COLOR DOPPLEit II\fTF~ltOPEE~4.TP:/E OLTRASOU:ND ft\! PAR,El'lCHYlVIAL SPA_RING STJRGER:!
mors or solitary tumors with limited normal renal function.12· 13 We evaluated patients with von Hippel-Lindau disease as part of a strategy to identify the von Rippel-Lindau disease gene. 6 Bilateral renal carcinomas develop in 60 to 75% of patients with von Rippel-Lindau disease and renal lesions. 4 • 11 • 18 • 19 While these tumors can be of low grade if detected early through screening of affected kindreds, metastases from renal carcinoma represent a major cause of death in von Rippel-Lindau disease patients. 7 - 9 We have also seen patients with metastatic renal cancer undergo remission after interleukin-2 based treatments and subsequently have isolated renal metastases. 20 Intraoperative ultrasound was helpful in characterizing the multiple, bilateral tumors or solitary deep sporadic lesions present in these patient groups. Preoperative CT and operative visualization of the kidney identified most (332 of 338) renal lesions. We found intraoperative ultrasound useful in the examination, localization or removal of a small subset (7%) of renal lesions identified previously. Gray scale sonograms were used to characterize lesions that were indeterminate on preoperative studies and to localize lesions demonstrated by preoperative studies but not apparent in the operating room.2· 3 We used a 5 MHz. transducer to visualize deep renal lesions. Adequate coupling was achieved by filling the incision with water or saline. Transducer artifact was not a problem, since the region of interest was the deeper aspect of the renal tumors. A superficial lesion was examined by moving the transducer to an adjacent area or to the other side of the kidney. Solid renal lesions in the hilum or deep in the renal parenchyma were examined with intraoperative ultrasound to evaluate the margin of normal tissue, which defines the resection and any vital adjacent structures. Color Doppler ultrasound identified arteries, veins and the urinary collecting system near the potential resection site, and estimated the thickness of renal parenchymal margin between the tumor and vessel. In 3 operations (11%) intraoperative ultrasound determined that there were no immediately adjacent renal vessels and that a lesion could be removed without the need for renal hypothermia, sparing unnecessary renal hilar dissection. Intraoperative ultrasound was also used in 1 patient to evaluate a renal vein thrombus not identified on preoperative studies. The use of intraoperative ultrasound to identify a renal vein thrombus in patients with renal cell carcinoma has already been reported. 4 Our experience demonstrates the spectrum of use ofintraoperative ultrasound in select lesions as an aid to renal parenchymal sparing surgery in general and in patients with von Rippel-Lindau disease in particular, and in the evaluation of unexpected renal vein thrombus. Judicious use of intraoperative ultrasound on lesions that are more difficult to resect can alter the surgical technique and decrease blood loss. Intraoperative ultrasound can be performed to evaluate the margin of large infiltrative lesions, when the surgical margin is not always apparent and when there is known to be a risk of small satellite tumors. 13 • 21 In these patients an adequate margin can be described by intraoperative ultrasound and satellite lesions can be removed. The use of intraoperative ultrasound was complimentary to and further refined the data obtained by the preoperative evaluation. We found intraoperative ultrasound to be particularly helpful in characterizing deep parenchymal cystic lesions and evaluating larger deep or hilar solid tumors. In our hands, intraoperative ultrasound was a tool to minimize blood and renal parenchymal loss, allowing safe removal of a renal lesion and subsequent pathological diagnosis. We recommend a high frequency color Doppler transducer to provide greater anatomical resolution of the tumor, margin of resection and surrounding structures. Intraoperative ultrasound performed before closure in patients with many renal lesions ensures that the kidney is thoroughly inspected, thus maximizing the benefit from each operation.
1987
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