Vascular Specificity in Differentiating Adrenal Carcinoma from Renal Cell Carcinoma 1
Diagnostic Radiology
Peggy Fritzsche, M.D., Charlene Andersen, M.D., and Patrick Cahill, M.D. Cases of adrenal and renal cell carcinoma were reviewed to evaluate vascular origin and architecture. All 9 cases of adrenal carcinoma showed fine, sparse neovascularity. Coarse, or at least extensive, neovascularity was demonstrated in 40 of 45 cases of renal cell carcinoma. An analysis of the angiographic features correlated with the known anatomical variations will nearly always enable one to ascertain the origin of the tumor. I NI:::EX TERMS: Adrenals, angiography • Adrenals, neoplasms, 8[6] .324 • Kidney neoplasms, angiography. (Renal cell carcinoma, 8[1].324) Radiology 125: 113-117, October 1977
ANATOMY
ESPITE THE USE of computed tomography to assess the retroperitoneum, the differentiation of adrenal from upper pole renal carcinoma is still challenging. Aortography with selective angiography remains valuable for this differentiation. We reviewed the angiographic vascular patterns of these two types of neoplasms; pertinent diagnostic information is obtained when the complex adrenal-renal arterial supply is understood and the neovascular architectural patterns recognized.
D
In a detailed anatomical study, Merklin and Michels (6) discussed the variable and complex vascularity of the kidney and adrenal gland. The kidney receives its blood
MATERIAL AND METHODS Cases of adrenal and renal cell carcinoma were selected from those assessed by aortography and selective angiography for an analysis of the vascular supply and the neovascular characteristics. The angiographic features evaluated were: (a) displacement of vessels (splaying or crowding); (b) lumen size and number of vessels; (c) arteriovenous shunting and "puddling" (ill-defined contrast accumulations); and (d) parasitic supply. The evaluation of lumen size and vessel number was based on comparisons with the opposite side and previous experience. A coarse vascular pattern was assigned to tumors showing increased lumen size. An extensive pattern was used to describe tumors with an increased number of vessels but no increase in the lumen diameter. The fine vascular pattern was used to refer to lumen diameter not greater than normal. The vascular characteristics of renal cell carcinoma are listed in TABLE I. Forty of the 45 cases revealed coarse or extensive neovascularity. Five hypovascular renal neoplasms were found. Approximately 26 % of the renal cases demonstrated parasitic blood supply, and greater than 50 % had puddling. The nine adrenal carcinomas displayed a fine sparse arterial pattern with splaying of the vessels.
Fig. 1. Typical adrenal carcinoma vascularity. An epinephrineenhanced selective renal angiogram shows accentuation of the typical fine adrenal neovascularity and constriction of the normal intrarenal branches.
1 From the Departments of Radiation Sciences, Loma Linda University School of Medicine, Loma Linda, Calif. (P.F., C.A.), and UCLA School of Medicine, Los Angeles, Calif. (P.C.). Presented at the Sixty-Second Scientific Assembly and Annual Meeting of the Radiological Society of ss North America, Chicago, III., Nov. 14-19, 1976.
113
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supply directly from the aorta; the adrenal gland has multiple arterial sources. Classically, the superior adrenal branches originating from the inferior phrenic artery supply the superomedial portion of the adrenal gland; middle adrenal branches directly from the aorta supply the anteromedial aspect of the gland; and inferior adrenal branches from the renal artery feed the posterior inferolateral portion. The adrenal arteries are multiple and extremely variable in origin. The inferior adrenal artery may arise from the aorta directly, from a segmental renal artery,
October 1977
from a renal capsular branch, or even from a gonadal artery. The inferior phrenic arteries usually arise from the aorta or celiac axis, but may show inconstant origin from the left gastric, hepatic, superior mesenteric, renal, or gonadal arteries. The vascular supplies of the kidney and adrenal gland are intimately related, and may communicate with all of the retroperitoneal structures through the arterial plexus of Turner. The superior renal capsular and inferior adrenal arteries frequently have a common origin from the renal
Fig. 2. Typical renal cell carcinoma vascularity. A. A selective renal angiogram demonstrates typical coarse neovascularity. B. A selective inferior adrenal angiogram shows hypertrophy of the artery in its usual anatomic location, and an extensive parasite contribution to the primary tumor area.
. Fig. 4. Adrenal-capsular complex. A. A selective renal angiogram shows enlarged adrenal-capsular vessels (arrow) displaced away from the kidney, indicating a neoplasm of renal origin. Capsular arteries commonly supply renal carcinomas, even when intracapsular in location. B. A selective renal angiogram demonstrates fine adrenal-capsular vessels displaced toward the kidney, consistent with a neoplasm of adrenal origin. Note that the margin of the superior pole is intact.
.
DIFFERENTIATING ADRENAL FROM RENAL CARCINOMA
Vol. 125
TABLE
I:
115
Diagnostic Radiology
RENAL CELL CARCINOMA VASCULAR CHARACTERISTICS
Coarse Extensive Hypovascular
25 15
Parasite 12/45 Puddling 24/45
5 45
artery or aorta, and either may give off a small renal polar branch. There are also potential anastomoses between intrarenal and perirenal arteries via the perforating middle capsular branches (Fig. 3). DISCUSSION
Adrenal carcinomas have a finely reticulated and sparse neovascular network, with minimal puddling or shunting (Fig. 1). Even though large adrenal neoplasms may present (in aortograms) as avascular lesions, increased neovascularity may be demonstrated via direct adrenal catheterization or with selective renal and inferior phrenic vasoconstriction (4). The vascularity is only increased relative to normal adrenal vessels, however, and does not approach the degree of hypervascularity typical of a renal cell carcinoma. The renal cell neoplasm characteristically has extensive coarse vessels, with moderate to severe puddling and shunting (Fig. 2). The low vascular resistance (due to hemodynamically effective arteriovenous shunts) attracts additional blood flow, and is reflected by increased arterial anastomoses (11). In contradistinction, the lack of arteriovenous shunting and less prominent puddling associated
Fig. 3. Unusual adrenal carcinoma vascularity. The fine, sparse neovascularity is supplied primarily by the inferior adrenal artery (arrow). An unusual contribution from the perforating middle capsular branch (curved arrow) perhaps reflects well-vascularized adhesions.
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with adrenal carcinomas requires less collateral flow, and thus the adrenal neoplasms never have the extensive hypervascular pattern of renal cell carcinomas. Neoplasms receive their dominant arterial supply from their organ of origin; it is therefore important to identify the primary feeding artery and to be familiar with the adrenal-renal vascular variations. Parasitic tumor blood supply is a frequent feature of renal cell carcinoma, but it is rarely
October 1977
found in cases of adrenal carcinoma. Initially, arterial supply to renal tumors from extrarenal sources was considered evidence of extension beyond the capsule (3, 5, 10). It is now known that collateral tumor supply does not necessarily indicate extracapsular extension (1, 2, 8, 11). Characteristically, renal neoplasms (even though intracapsular) will have a blood supply augmented by enlarged anastomotic vessels which are otherwise normal in their
Fig. 5. Hypovascular renal cell carcinoma. A. A selective renal angiogram fails to demonstrate the vascular supply of the upper pole renal cell carcinoma (arrowheads). The small inferior adrenal artery (curved arrow) is displaced around a renal hilar mass which was documented at surgery to be an extrarenal tumor. B. A later phase selective renal angiogram shows that the small inferior adrenal-capsular plexus (curved arrow) is displaced toward the intrarenal mass, but it does not participate in the primary tumor vasculature. C. An epinephrine-enhanced selective renal angiogram shows splaying of the upper pole intrarenal branch to encompass the primary tumor mass (arrowheads). There is reflux filling of several lumbar arteries, responsible for the neovascularity in the renal hilus (curved arrow). Neovascularity in the usual area of distribution of the lumbar arteries indicates extracapsular tumor extension.
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DIFFERENTIATING ADRENAL FROM RENAL CARCINOMA
own anatomic locations and show neovascularity only in the primary tumor area. However, identification of neovascularity outside the kidney or main tumor area (in the usual distribution of the contributing artery) is consistent with extracapsular extension (8). Neoplasms are known to stimulate a proliferative fibroblastic and vascular response resulting in well-vascularized adhesions, as demonstrated in a reported case of adrenal carcinoma (11). An inflammatory response may have been a factor in the adrenal carcinoma vascularity acquired through a perforating capsular branch in one of our cases (Fig. 3). Two adrenal neoplasms, one a pheochromocytoma and one a carcinoma, have been reported as showing a dominantly renal supply (9). Both were located laterally on the renal surface, and did not significantly displace intrarenal vessels. The one adrenal carcinoma described by Shrago et al. (9) retained the fine sparse vasculature common to all of our adrenal carcinomas located in the typical suprarenal position. More than half of all renal carcinomas are supplied by capsular arteries (8). Capsular artery displacement (7) will be away from the kidney when the tumor has renal origin, and toward the kidney if the origin is adrenal (Fig. 4). The usual flow in the perforating middle capsular arteries is from intrarenal to perirenal, but is easily reversed when the intrarenal demand is increased (1, 2). Collateral pathways are commonly visualized in cases of renal cell carcinoma, arteriovenous malformation, and renal arterial occlusive disease. Hypovascular renal cell carcinomas provide an additional challenge when located superiorly because of their sparse neovasculature (similar to that in adrenal carcinomas). Even though the tumor vascularity is not striking,
117
Diagnostic Radiology
it is visualized simultaneously with the renal vessels and extends directly from an interlobar branch. Renal-origin arterial supply is also indicated by the splaying of intrarenal branches to encompass the tumor mass (Fig. 5). ACKNOWLEDGMENT: We wish to thank Robert L. Waldron II, M.D., Director of Radiology, French Hospital, San Luis Obispo, California, for the use of the case shown in Figure 5.
Department of Radiation Sciences Lorna Linda University School of Medicine Lorna Linda, Calif. 92354
REFERENCES 1. Brindle MJ: Alternative vascular channels in renal cell carcinoma. Clin Radiol 23:321-330, Jul 1972 2. Buist TS: Parasitic arterial supply to lntracapsular renal cell carcinoma. Am J RoentgenoI120:653-659, Mar 1974 3. Kahn PC, Frates RE: The value of angiography of the small branches of the abdominal aorta. Am J Roentgenol 102:407-417, Feb 1968 4. Kahn PC, Nickrosz LV: Selective angiography of the adrenal glands. Am J RoentgenoI101:739-749, Nov 1967 5. Lang EK: Arterial assessment and staging of renal cell carcinoma. Radiology 101:17-27, Oct 1971 6. Merklin RJ, Michels NA: Variant renal and suprarenal blood supply with data on inferior phrenic, ureteral and gonadal arteries: statistical analysis based on 185 dissections and review of literature. J Int Coli Surg 29:41-76, Jan 1958 7. Meyers MA, Friedenberg RM, King MC, et al: The significance of the renal capsular arteries. Br J Radiol 40:949-956, Dec 1967 8. Ruzicka FF, Rossi P, Abrams RE, et al: Anomalous and parasitic arterial blood supply in the abdomen. Radiology 96:261-268, Aug 1970 9. Shrago00, McKinnon CM, Clark R: Adrenal tumors simulating intrarenal lesions. Am J Roentgenol 121:518-522, Jul 1974 10. Sondag TJ, Petasnick JP, Patel SK, et al: Hypernephromas with parasitic blood supply derived from the superior and inferior mesenteric arteries. Radiology 103:509-513, Jun 1972 11. Sprayregen S: Parasitic blood supply of neoplasms. Radiology 106:529-535, Mar 1973
Diagnostic Radiology
Peggy Fritzsche, M.D., Charlene Andersen, M.D., and Patrick Cahill, M.D. Cases of adrenal and renal cell carcinoma were reviewed to evaluate vascular origin and architecture. All 9 cases of adrenal carcinoma showed fine, sparse neovascularity. Coarse, or at least extensive, neovascularity was demonstrated in 40 of 45 cases of renal cell carcinoma. An analysis of the angiographic features correlated with the known anatomical variations will nearly always enable one to ascertain the origin of the tumor. I NI:::EX TERMS: Adrenals, angiography • Adrenals, neoplasms, 8[6] .324 • Kidney neoplasms, angiography. (Renal cell carcinoma, 8[1].324) Radiology 125: 113-117, October 1977
ANATOMY
ESPITE THE USE of computed tomography to assess the retroperitoneum, the differentiation of adrenal from upper pole renal carcinoma is still challenging. Aortography with selective angiography remains valuable for this differentiation. We reviewed the angiographic vascular patterns of these two types of neoplasms; pertinent diagnostic information is obtained when the complex adrenal-renal arterial supply is understood and the neovascular architectural patterns recognized.
D
In a detailed anatomical study, Merklin and Michels (6) discussed the variable and complex vascularity of the kidney and adrenal gland. The kidney receives its blood
MATERIAL AND METHODS Cases of adrenal and renal cell carcinoma were selected from those assessed by aortography and selective angiography for an analysis of the vascular supply and the neovascular characteristics. The angiographic features evaluated were: (a) displacement of vessels (splaying or crowding); (b) lumen size and number of vessels; (c) arteriovenous shunting and "puddling" (ill-defined contrast accumulations); and (d) parasitic supply. The evaluation of lumen size and vessel number was based on comparisons with the opposite side and previous experience. A coarse vascular pattern was assigned to tumors showing increased lumen size. An extensive pattern was used to describe tumors with an increased number of vessels but no increase in the lumen diameter. The fine vascular pattern was used to refer to lumen diameter not greater than normal. The vascular characteristics of renal cell carcinoma are listed in TABLE I. Forty of the 45 cases revealed coarse or extensive neovascularity. Five hypovascular renal neoplasms were found. Approximately 26 % of the renal cases demonstrated parasitic blood supply, and greater than 50 % had puddling. The nine adrenal carcinomas displayed a fine sparse arterial pattern with splaying of the vessels.
Fig. 1. Typical adrenal carcinoma vascularity. An epinephrineenhanced selective renal angiogram shows accentuation of the typical fine adrenal neovascularity and constriction of the normal intrarenal branches.
1 From the Departments of Radiation Sciences, Loma Linda University School of Medicine, Loma Linda, Calif. (P.F., C.A.), and UCLA School of Medicine, Los Angeles, Calif. (P.C.). Presented at the Sixty-Second Scientific Assembly and Annual Meeting of the Radiological Society of ss North America, Chicago, III., Nov. 14-19, 1976.
113
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PEGGY FRITZSCHE AND OTHERS
supply directly from the aorta; the adrenal gland has multiple arterial sources. Classically, the superior adrenal branches originating from the inferior phrenic artery supply the superomedial portion of the adrenal gland; middle adrenal branches directly from the aorta supply the anteromedial aspect of the gland; and inferior adrenal branches from the renal artery feed the posterior inferolateral portion. The adrenal arteries are multiple and extremely variable in origin. The inferior adrenal artery may arise from the aorta directly, from a segmental renal artery,
October 1977
from a renal capsular branch, or even from a gonadal artery. The inferior phrenic arteries usually arise from the aorta or celiac axis, but may show inconstant origin from the left gastric, hepatic, superior mesenteric, renal, or gonadal arteries. The vascular supplies of the kidney and adrenal gland are intimately related, and may communicate with all of the retroperitoneal structures through the arterial plexus of Turner. The superior renal capsular and inferior adrenal arteries frequently have a common origin from the renal
Fig. 2. Typical renal cell carcinoma vascularity. A. A selective renal angiogram demonstrates typical coarse neovascularity. B. A selective inferior adrenal angiogram shows hypertrophy of the artery in its usual anatomic location, and an extensive parasite contribution to the primary tumor area.
. Fig. 4. Adrenal-capsular complex. A. A selective renal angiogram shows enlarged adrenal-capsular vessels (arrow) displaced away from the kidney, indicating a neoplasm of renal origin. Capsular arteries commonly supply renal carcinomas, even when intracapsular in location. B. A selective renal angiogram demonstrates fine adrenal-capsular vessels displaced toward the kidney, consistent with a neoplasm of adrenal origin. Note that the margin of the superior pole is intact.
.
DIFFERENTIATING ADRENAL FROM RENAL CARCINOMA
Vol. 125
TABLE
I:
115
Diagnostic Radiology
RENAL CELL CARCINOMA VASCULAR CHARACTERISTICS
Coarse Extensive Hypovascular
25 15
Parasite 12/45 Puddling 24/45
5 45
artery or aorta, and either may give off a small renal polar branch. There are also potential anastomoses between intrarenal and perirenal arteries via the perforating middle capsular branches (Fig. 3). DISCUSSION
Adrenal carcinomas have a finely reticulated and sparse neovascular network, with minimal puddling or shunting (Fig. 1). Even though large adrenal neoplasms may present (in aortograms) as avascular lesions, increased neovascularity may be demonstrated via direct adrenal catheterization or with selective renal and inferior phrenic vasoconstriction (4). The vascularity is only increased relative to normal adrenal vessels, however, and does not approach the degree of hypervascularity typical of a renal cell carcinoma. The renal cell neoplasm characteristically has extensive coarse vessels, with moderate to severe puddling and shunting (Fig. 2). The low vascular resistance (due to hemodynamically effective arteriovenous shunts) attracts additional blood flow, and is reflected by increased arterial anastomoses (11). In contradistinction, the lack of arteriovenous shunting and less prominent puddling associated
Fig. 3. Unusual adrenal carcinoma vascularity. The fine, sparse neovascularity is supplied primarily by the inferior adrenal artery (arrow). An unusual contribution from the perforating middle capsular branch (curved arrow) perhaps reflects well-vascularized adhesions.
116
PEGGY FRITZSCHE AND OTHERS
with adrenal carcinomas requires less collateral flow, and thus the adrenal neoplasms never have the extensive hypervascular pattern of renal cell carcinomas. Neoplasms receive their dominant arterial supply from their organ of origin; it is therefore important to identify the primary feeding artery and to be familiar with the adrenal-renal vascular variations. Parasitic tumor blood supply is a frequent feature of renal cell carcinoma, but it is rarely
October 1977
found in cases of adrenal carcinoma. Initially, arterial supply to renal tumors from extrarenal sources was considered evidence of extension beyond the capsule (3, 5, 10). It is now known that collateral tumor supply does not necessarily indicate extracapsular extension (1, 2, 8, 11). Characteristically, renal neoplasms (even though intracapsular) will have a blood supply augmented by enlarged anastomotic vessels which are otherwise normal in their
Fig. 5. Hypovascular renal cell carcinoma. A. A selective renal angiogram fails to demonstrate the vascular supply of the upper pole renal cell carcinoma (arrowheads). The small inferior adrenal artery (curved arrow) is displaced around a renal hilar mass which was documented at surgery to be an extrarenal tumor. B. A later phase selective renal angiogram shows that the small inferior adrenal-capsular plexus (curved arrow) is displaced toward the intrarenal mass, but it does not participate in the primary tumor vasculature. C. An epinephrine-enhanced selective renal angiogram shows splaying of the upper pole intrarenal branch to encompass the primary tumor mass (arrowheads). There is reflux filling of several lumbar arteries, responsible for the neovascularity in the renal hilus (curved arrow). Neovascularity in the usual area of distribution of the lumbar arteries indicates extracapsular tumor extension.
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DIFFERENTIATING ADRENAL FROM RENAL CARCINOMA
own anatomic locations and show neovascularity only in the primary tumor area. However, identification of neovascularity outside the kidney or main tumor area (in the usual distribution of the contributing artery) is consistent with extracapsular extension (8). Neoplasms are known to stimulate a proliferative fibroblastic and vascular response resulting in well-vascularized adhesions, as demonstrated in a reported case of adrenal carcinoma (11). An inflammatory response may have been a factor in the adrenal carcinoma vascularity acquired through a perforating capsular branch in one of our cases (Fig. 3). Two adrenal neoplasms, one a pheochromocytoma and one a carcinoma, have been reported as showing a dominantly renal supply (9). Both were located laterally on the renal surface, and did not significantly displace intrarenal vessels. The one adrenal carcinoma described by Shrago et al. (9) retained the fine sparse vasculature common to all of our adrenal carcinomas located in the typical suprarenal position. More than half of all renal carcinomas are supplied by capsular arteries (8). Capsular artery displacement (7) will be away from the kidney when the tumor has renal origin, and toward the kidney if the origin is adrenal (Fig. 4). The usual flow in the perforating middle capsular arteries is from intrarenal to perirenal, but is easily reversed when the intrarenal demand is increased (1, 2). Collateral pathways are commonly visualized in cases of renal cell carcinoma, arteriovenous malformation, and renal arterial occlusive disease. Hypovascular renal cell carcinomas provide an additional challenge when located superiorly because of their sparse neovasculature (similar to that in adrenal carcinomas). Even though the tumor vascularity is not striking,
117
Diagnostic Radiology
it is visualized simultaneously with the renal vessels and extends directly from an interlobar branch. Renal-origin arterial supply is also indicated by the splaying of intrarenal branches to encompass the tumor mass (Fig. 5). ACKNOWLEDGMENT: We wish to thank Robert L. Waldron II, M.D., Director of Radiology, French Hospital, San Luis Obispo, California, for the use of the case shown in Figure 5.
Department of Radiation Sciences Lorna Linda University School of Medicine Lorna Linda, Calif. 92354
REFERENCES 1. Brindle MJ: Alternative vascular channels in renal cell carcinoma. Clin Radiol 23:321-330, Jul 1972 2. Buist TS: Parasitic arterial supply to lntracapsular renal cell carcinoma. Am J RoentgenoI120:653-659, Mar 1974 3. Kahn PC, Frates RE: The value of angiography of the small branches of the abdominal aorta. Am J Roentgenol 102:407-417, Feb 1968 4. Kahn PC, Nickrosz LV: Selective angiography of the adrenal glands. Am J RoentgenoI101:739-749, Nov 1967 5. Lang EK: Arterial assessment and staging of renal cell carcinoma. Radiology 101:17-27, Oct 1971 6. Merklin RJ, Michels NA: Variant renal and suprarenal blood supply with data on inferior phrenic, ureteral and gonadal arteries: statistical analysis based on 185 dissections and review of literature. J Int Coli Surg 29:41-76, Jan 1958 7. Meyers MA, Friedenberg RM, King MC, et al: The significance of the renal capsular arteries. Br J Radiol 40:949-956, Dec 1967 8. Ruzicka FF, Rossi P, Abrams RE, et al: Anomalous and parasitic arterial blood supply in the abdomen. Radiology 96:261-268, Aug 1970 9. Shrago00, McKinnon CM, Clark R: Adrenal tumors simulating intrarenal lesions. Am J Roentgenol 121:518-522, Jul 1974 10. Sondag TJ, Petasnick JP, Patel SK, et al: Hypernephromas with parasitic blood supply derived from the superior and inferior mesenteric arteries. Radiology 103:509-513, Jun 1972 11. Sprayregen S: Parasitic blood supply of neoplasms. Radiology 106:529-535, Mar 1973
