- Email: [email protected]
Angiography of hepatic neoplasms: A review
Int. f. Rodiation
Oncolog~
Biel.
Phys.,
1976. Vol.
1. pp. 965-971.
ANGIOGRAPHY
Pergamon
of Radiology.
Printed
OF HEPATIC A REVIEW
DAVID Department
Pres.
University
G.
in the
U.S.A.
NEOPLASMS:
BRAGG, M.D.
of Utah Medical U.S.A.
Center,
Salt Lake City. UT 84132.
Selective angiographic techniques provide the clinician with another method to evaïuate the Ever for space occupying lesions. Basicahy, tumor vascularity, wen more than size, is the critical factor in the angiographic expression of these mass lesions. The typical hepatoma, solitary and multfnodular forms, usually is visuahzed with ease. More often, scirrhous cholangiocarcinoma is a much more diicult angiographic diagnosis, since less dramatic vascular changes are associated with it. Of the metastatic tumors to the liver, dfffuse adenocarcinoma secondaries from the GI tract are more common, and show iess vivid vascular changes. Since al1 neoplasms of the liver derive their vascuiar supply from hepatic arteries, the late phase of the angiogram or the portogram wil1 show negative filling defects, occasionally as smal1 as 1 cm in size. Since these filling defects are non-spec&, the arteriographic changes subsequent to the tumor must be evahtated carefully to make a specific diagnosis. The arteriographic features of some benign Ever tumors are mentioned, only in a dferential setting, since they usualty can be distinguished from their maiignant counterparts. The exceptfon to this latter statement is the liver cell adenoma which resembles a hepatoma angiographically. Hepatic neoplasms,
PLAIN
FILM
Angiography,
Tumor
vascularity,
PINDINGS
Metastatic
liver disease.
sites reported to be associated with calcified metastatic liver lesions have been ovarian serous cystadenocarcinoma, neuroblastoma, breast and lung carcinomas, and melanoma.’
film of the abdomen plays a small, but occasionally dramatic role in the diagnosis of hepatic neoplasms. In benign lesions, the caverneus hemangioma uncommonly may calcify, usually with amorphous calcium deposits within the fibrous septa of the tumor. It is quite rare to observe phleboliths within Of the primary malignant hemangiomas.” hepatic tumors, the hepatoma most frequently contains sufficient calcium to be visible radiographically, an event more commonly noted in those tumors presenting in childWhen seen, the calcium deposits hood.” appear as a dense, tumoral mass. Of the metastatic hepatic tumors, a number of lesions may be visible on plain films. As a group, the mucin producing adenocarcinomas are said to contain calcium most frequently. They may occur anywhere in the GI tract? but are found most often in the left colon. Other primary
Bierman et aL5 first reported the successful catheterization of the celiac and superior mesenteric arteries in the evaluation of liver disease, together with the angiographic features of liver tumors. After the present technique for selective arterial catheterization was introduced in 1953, hepatic angiography became an acceptable, low risk method for the evaluation of liver abnormalities.4 A discussion of angiographic equipment, techniques, anatomy and complications appears in Stilberg and Bierman.z1 Both primary and metastatic hepatic tumors receive their blood supply from the hepatic
Acknowledgement-The efforts of Dr. P. Ruben
offering many helpful suggestions ment of this review paper.
The
plain
author Koehler
appreciates in reviewing
the and
ANGIOGRAPHIC PROCEDURES TERMINOLOGY
965
AND
in the develop-
966
Radiation Oncology 0 Biology 0 Physics
September-October
arterial tree. Study of the hepatic venous system seldom is of value in the workup of liver neoplasms because the direction of blood flow is away from the liver. Opacification of the portal venous system does have value in this disease setting, both with regard to displacement and involvement of the portal system from the neoplasm as wel1 as in the delineation of the mass lesion as a “negative” filling defect(s) during the portogram phase. Since no tumor derives any significant portion of its blood supply from the portal circulation, the site of the neoplasm always appears as a “negative” defect regardles of etiology. In approximately 50% of cases with known liver space occupying masses, the portogram phase of the angiographic study wil1 reveal their presence.” The threshold size of a lesion for detection is estimated to be 1 cm, but in practice, the lesion must usually be larger to be seen. Tumor vascularity, not size is the critical factor in allowing angiographic diagnosis, as wil1 be explained later. The angiographic approach to the portal venous system now is either by catheterization directly of its tributaries or subsequent to the injection of the splenic or superior mesenteric arterial tree. The more hazardous direct splenic pulp injections have been abandoned largely in favor of these safer catheter approaches. Priscoline injected into the superior mesenteric artery enhances the subsequent portal vein opacification. An understanding of the angiographic patterns of the different primary and metastatic hepatic neoplasms can be complimented with a knowledge of their histopathologie composition. This discussion wil1 focus on the hepatic cel1 type (hepatoma) and the duet cel1 malignant primary (cholangiocarcinoma) eithelial tumors. Although pathologie examples of mixed tumors are reported, the dominant cel1 type largely determines their clinical and angiographic characteristics. The benign hepatic neoplasms wil1 be discussed only in a differential setting. The reader is referred to the bibliography for a more in depth discussion of these entities.“‘.‘5.‘6 To the individual not familiar with angiographic terminology, a brief glossary seems appropriate. “Cuffing” of vessels refers to
1976, Vol. 1, Number 9 and Number 10
irregular narrowing of arteries as a result of tumor encasement. It is more commonly seen in primary tumors but may occur in metastatic lesions as well. Tumor vessels are the angiographic expression of neovascularity. These arteries develop in response to the tumor and are unique physiologically in lacking a smooth muscle cuff capable of responding to vasoconstrictive drugs. This latter feature allows the use of vasoactive agents to enhance the angiographic appearance of a tumor by diminishing or obliterating the non-neoplastic, normal arterial bed. Angiographically tumor vessels are characterized by disorganization. They widen and narrow irregularly and branch in a non-random manner, leading to the formation of irregular contrasts pools or lakes. A “tumor stain” is an abnormality observed during the capillary phase of the angiographic within the study.24 Contrast concentrations tumor capillary bed create a blush which tends to correlate both with the size and vascularity of the primary or metastatic lesion. Arteriovenous shunting refers to early venous filling. It is an infrequently observed angiographic abnormality which, with increased arterial flow, is more commonly seen with primary hepatic cel1 tumors; however it also occasionally may be noted in the presence of metastatic disease to the liver.“.24 “Corkscrew vessels” is the descriptive label given to the appearance of the arterial tree of the end stage cirrhotic liver. It is a non-specific observation, produced by any condition associated with marked contracture of liver volume, of which cirrhosis is, of course, the most common.*.*’ “Draping” of vessels refers to the non-specific displacement of the arteries and veins around a mass lesion (Fig. 1). The first angiographic step in the evaluation of an hepatic mass lesion is the determination of its location within the liver. This may not always be an easy task in spite of the criteria outlined by Rossi and Ruzicka.*’ Extrahepatic mass lesions, on occasion, exactly mimic the appearance of intrahepatic tumors, necessitating the injection of neighboring arteries and requiring the use of additional projections to aid in this differentiation.*’ The purposes of hepatic angiography are not only in establishing the presence and
Angiography
of hepatic neoplasms
0 D. CT. BRAGG
967
The potential communications between the celiac and superior mesenteric systems frequently are recruited in instances of occlusive vascular disease as well. Knowledge of these vascular variations is vita1 to the angiographer as wel1 as the surgeon and oncologist when planning resection or perfusion of hepatic malignancies.
Fig. 1. Patient JS-This 44 year old male presented with a history of amoebic hepatitis diagnosed subsequent to his return from Korea. A positive liver scan led to this angiogram which demonstrates extensive tumor replacement principally involving the right lobe of the liver, but also extending to the left lobe. A discrete mass in the subphrenic area of the liver represents the largest vascular tumor (single arrow t ) with smaller lesions identified by the double arrow ( T T ) in the inferior and lateral margin of the liver as wel1 as centrally in the right lobe. This multicentric lesion is malignant angiographically and felt consistent, either with a multicentric hepatoma or a vascular metastatic lesion such as a carcinoid tumor. At surgery a multifocal hepatoma was found. This tumor characterizes the vivid angiographic alterations of the solitary massive hepatoma and shows examples of tumor vessels and “draping” of vessels.
nature of hepatic mass lesions, but also in defining the extent of involvement and outlining the vascular roadmaps for possible hepatic resection or chemotherapeutic perfusion. It should be recalled that in approximately 16% of cases, the right hepatic artery arises from the superior mesenteric artery. Similarly. there is an 18% incidence of the left hepatic artery arising from the left gastric branch.‘O
PRIMARY LIVER TUMORS YuZ7 has reported a large angiographic series of 50 hepatomas and divided the tumors into three gross patterns: solitary massive (8 cases), nodular (10 cases) and diffuse (32 cases). The most dramatic angiographic patterns were described in the solitary massive and diffuse forms (increased vascularity, tumor vessels, tumor stain, A-V shunting). Dilation of the hepatic artery was noted in al1 50 cases, presumably as a reflection of the increased vascular demand by the tumor. Using a different approach, Kido, Sasaki and Kaneko13 correlated the histologie types of the primary malignant hepatic epithelial tumors with their angiographic characteristics. In the wel1 differentiated hepatomas (24 cases), al1 showed tumor vessels, with the majority revealing both tumor stains and A-V shunting (19 of 24 and 17 of 24 respectively). Of the anaplastic hepatomas (six cases). tumor vessels and tumor stains were noted in four and A-V shunting in one. Of the seven cholangiocarcinomas, tumor vessels and tumor staining characterized four, however, none were noted to have A-V shunting. The angiographic similarity between anaplastic hepatomas and cholangiocarcinomas is suggested by these observations. Using the above defined criteria of Yu, Gammill et al.’ proposed an angiographic scheme useful in predicting the aggressiveness and extent of the primary hepatic tumor and the chances of its being respectable surgically. They suggest a chronologie trend in the evolution of angiographic changes in a malignant epithelial type hepatic tumor, from first developing tumor neovascularity, tumor blood pooling, then tumor staining and finally becoming avascular as the tumor outgrows its blood SUPPlY.
968
Radiation
Oncology
??Biology 0 Physics
September-October
1976, Vol. 1, Number 9 and Number
10
(bl (al
Figs. 2(a-c). An axillary selective right hepatic arterial injection shows a centra1 large mass lesion in the right lobe of the liver with vessels “draped” around the lesion (2a) throughout. The hepatogram phase (2b) demonstrates diffuse “tumor stains” irregularly throughout the right lobe of the liver (arrows). The transverse ultrasound scan (2~). B mode demonstrates the abnormal return echoes within the substance of the liver defining the largest of the space occupying lesion (arrows) solid by sonographic characteristics. The diagnosis was metastatic tumor from a primary in the colon, showing the vascular nature of these lesions similar to the multifocal hepatoma shown in Fig. 1. In contrast to the hepatic cel1 tumor, the bile duet primary tumors tend to be scirrhous in form, more invasive, with less of a mass and usually unimpressive tumor effect, These bile duet neoplasms neovascularity.6.iZ are quite obviously a greater angiographic challenge in diagnosis. Arterial encasement or rather than displacement or obstruction, “draping” is reported in 81%; the reverse is true with hepatomas. As cholangiocarcinomas arise most frequently near the junction of the
cystic and common ducts, a careful review of the angiogram may show smal1 beaded tumor vessels in the region of the liver hilus. In spite of the centra1 origin of cholangiocarcinomas, adjacent to the portal vein, this venous trunk seldom is involved by the tumor, yet commonly is obstructed with hepatomas (portal vein abnormalities are reported in 13% of cholangiocarcinomas in contrast to 45% of hepatomas.” An angiographic analogy exists with the primary renal tumors which is similar
Angiography of hepatic neoplasms 0 D. G. BRAGG
969
lasia and regenerating liver nodules in cirrhoto the cholangiocarcinoma: hepatoma model in the transitional cell: hypernephroma ar- tic patients, the scan serves as a diagnostic complement to the angiogram.7.‘6 teriographic patterns of presentation. The size threshold for the recognition of a Carcinoma of the gallbladder has proven to is smaller than be the diagnostic enigma with reference to the mass lesion angiographically the reported 2 cm lesion in the radionuclide biliary tree. The uncommon epidermoid form hepatogram; occasionally, it may approach of this tumor should provide a better arteriographic model; however, an adenocarcinoma is 1 cm. The vascularity of the primary tumor the more common histologie type. and it determines the angiographic expression of the usually presents in a scirrhous pattern, further metastatic lesions. Visualization also depends on the location of the lesion within the liver, limiting the angiographer’s ability to recognize gallbladder cancer. However, Abrams el al.’ as we11 as the extent of involvement present. Of the vascular metastatic hepatic lesions, the were able to diagnose correctly 6 cases following are included: hypernephromas, by selective celiac and superior mesenteric lieomyosarcomas, carcinoid tumors, islet cell angiography. In each example, the cystic and papillary cell tumors of the pancreas, and artery was enlarged with cuffing or amputation transitional cel1 tumors. Of the avascular of one of its branches. In addition, the angiographic metastatic lesions, adenocarabnormal tumor stain created a thick. uneven cinomas lead the list, specifically those of the gallbladder wal], feit to be specific for tumor. pancreas, and breast. Primary Extension to the liver from the primary site in stomach, tumors of the lung, adrenal gland and the gallbladder created an abnormal vascular melanoma also should be mentioned.‘b”’ pattern at the involved site. NO false positive Metastatic lesions have been reported to or negative examples were reported. In summary, the angiographer’s ability to mimic all of the angiographic changes of diagnose primary malignant hepatic tumors primary liver tumors. At the other extreme is the group of avascular metastatic lesions depends upon the degree of vascularity induced by the tumor. This can vary from described above which may show only an uneven hepatogram which of itself, is quite dramatic in the case of the solitary massive non-specific.* Other angiographic signs of hepatoma, to the very subtle or non-existent tumor must be visualized, particularly with angiographic changes with the cholangiocardiffuse metastatic disease, to be confident of cinema and gallbladder tumors. the diagnosis. METASTATIC LIVER DISEASE Of the benign hepatic neoplasms, the With regard to metastatic disease to the caverneus hemangioma is the most important liver, the angiographer must be concerned to recognize. This mass lesion may be single with his accuracy in the recognition of or multiple, large or smal], presenting with secondary tumors as we11 as his ability to impressively abnormal, increased vascularity. NO true tumor vessels or evidente for distinguish these lesions from primary maligvascular cuffing occurs with benign lesions. nant and benign hepatic lesions. Angiography clearly carries too great a risk and tost to be The delayed angiographic films reveal the diagnostic features of a caverneus hemanuseful as a routine screening procedure for the detection of metastatic disease.* The quoted gioma: late (lg-20 sec) pooling of contrast in angiographic accuracy approaches that of sinusoidal lakes found within these masses. radionuclide liver scanning in the detection of Their recognition is important as blind needle biopsy of these vascular lesions may be hepatic mass lesions, but is more specific.‘*.” Superselective and magnification angiographic disastrous.“.” Examples of f&al nodular hyperplasia of techniques as wel1 as pharmacologic aides the liver are said to show suficient angioghave improved this accuracy in recent years. At present, angiography serves as a means of raphic differences to allow their distinction from malignant tumors. These diff erences evaluation of the non-specific, abnormal relate to the feeding arteries which arise from radionuclide scan. With focal nodular hyperp-
970
Radiation
Oncology
0 Bioiogy
0 Physics
September-October
the periphery of the tumor, together with the absente of true tumor vessels, A-V shunting and portal vein invo1vement.7.‘0.‘6 Nuclear scanning in focal nodular hyperplasia wil1 fail to show a mass lesion, confirming the diagnosis. The angiographic features of liver cel1 adenoma usually are undistinguishable from those of a hepatoma. Infusion techniques have been introduced in an attempt to enhance the screening accuracy of the hepatic angiogram in the detection of mass lesions. This method is reported to allow for an improved accuracy in the diagnosis of mass lesions, but obviates the more specific means to recognize the arteriographic criteria of malignant hepatic primaries.25.26 In recent years, improvement in ultrasound imaging potential has provided yet another means of iiver imaging. This modality serves to compliment the above described angiog-
1976, Vol.
1. Number
9 and Number
10
raphic techniques, particularly with regard to the differentiation of cystic from solid tumor masses. In summary, hepatic arteriography has enhanced significantly the clinician’s ability to diagnose accurately and manage the patient with a mass lesion of the liver. As experience in this field has developed, both the limitations and the need for exquisite technique and film quality has been magnified. In perspective, the hepatic angiogram is the major diagnostic procedure in the pre-treatment evaluation of the patient suspected of having a primary liver tumor both with respect to the pre-biopsy localization and the pre-surgical definition. Although many benign and metastatic liver masses may have significant vascular abnormalities allowing their angiographic recognition, considerable experience and ski11 is required to specifically categorize and define them.
REFERENCES
Abrams, R.M., Meng, C.H., Firooznia, H., Beranbaum, E.R., Epstein, H.Y.: Angiographic
Bookstein, J.J., Appelman, H.D.: Angiographic findings in benign liver cel1 tumors. Radiology
demonstration of carcinoma of the gallbladder. Radiology 94: 277-282, 1970. 2. Alfidi, R.J., Rastogi, H., Buonocore, E., Brown, C.H.: Hepatic arteriography. Radiology 90: 1136-1142, 1%8. 3. Allen, R.W., Holt, A.H.: Calcification in primary liver carcinoma. Am. J. Roentgenol. 99: 150-152, 1967. 4. Baum, S.: Hepatic arteriography. Am. J. Gastroent. 51: 151-153, 1969. 5. Bierman, H.R., Miller, E.R., Bryon, Jr, R.L., Dod, K.S., Kelly, K.H., Black, D.H.: Intraarterial catheterization of viscera in man. Am. J. Roentgenol. 66: 555-568, 1951. 6. Boijsen, E., Abrams, H.L.: Roentgenologic diagnosis of primary carcinoma of liver. Acts Radiology (Diagn.) 3: 257-277, 1965. 7. Farrell, R., Steinman, A., Green, W.H.: Arteriovenous shunting in a regenerating liver simulating hepatoma. Radiology 102: 279-280, Feb. 1972. 8. Fredans, M., Egeblad, M., Holst-Nielsen, F.: The value of selective angiography in the diagnosis of tumors of the pancreas and liver. Radiology 93: 765-769, Oct. 1%9. 9. Gammill, S.L., Takahashi, M., Kawanami, M., ,Font, R., Sparks, R.: Hepatic angiography in the selection of patients with hepatomas for hepatic lobectomy. Radiology 101: 549-554, 1971. 10. Goldstein, H.M., Neiman, H.L., Mena, E.,
110: 339-343, Feb. 1974. 11. Jewel, K.L.: Primary carcinoma of the liver: clinical and radiologie manifestations. Am. J. Roentgenol. 113: 84-91, Sept. 1971. 12. Kaude, J., Rian, R.: Cholangiocarcinoma. Radiology 100: 573-580, Sept. 1971. 13. Kido, C., Sasaki, T., Kaneko, M.: Angiography of primary liver cancer. Am. J. Roentgenof. 113: 70-81, Sept. 1971. 14. McDonald, P.: Hepatic tumours in childhood. Clin. Radiol. 18: 74-82, 1%7. 15. McLoughlin, M.J.: Angiography in caverneus hemangioma of the liver. Am. J. Roentgenol. 113: 50-55, 1971. 16. McLoughlin, M.J., Colapinto, R.F., Gilday, D.L., Hobbs, B.B., Korobkin, M.T., McDonald, P., Phillips, M.J.: Focal nodular hyperplasia of the liver: angiography and radioisotope scanning. Radiology 107: 257-263, May 1973. 17. Mess, A.A., Clark, R.E., Palubinskas, A.J., DeLorimier, A.A.: Angiographic appearance of benign and malignant hepatic tumors in infants and children. Am. J. Roentgenol. 113: 61-69, 1971. 18. Nebesar, R.A., Pollard, J.J., Stone, D.L.: Angiographic diagnosis of malignant disease of the liver. Radiology 86: 284-292, 1%6. 19. Pollard, J.J., Fleischli. D.J., Nebesar, R.A.: Angiography of hepatic neoplasms. Rad. Clinics North Am. 8: 3141, Apr. 1970. 20. Pollard, J.J., Nebesar, R.A.: Abdominal angiog-
1.
Angiography
of hepatic neoplasms
raphy. N. Eng1 J. Med. I 279: 1093-1100. 14 Nov. 1%8: 11 279: 1148-1152, 21 Nov. 1%8. 21. Rossi, P.. Ruzicka. F.F.: Differentiation of intrahepatic and extrahepatic masses by arteriography. Radiology 93: 771-780, Oct. 1969. 22. Shanser, J.D., Glickman. M.G.. Palubinskas, A.J.: Pitfalls in the arteriographic differentiation of intrahepatic anc extrahepatic masses. Am. J. Roentgenol. 121: 420-429, June 1974. 23. Stulberg. H.J. Bierman. H.R.: Selective hepatic arteriography: normal anatomy, anatomie variation, pathologie conditions. Radiology 85:
46-55, 1%5. 24. Watson. R.C., Baltaxe, H.A.: The angiographic
0 D. G. BRAGG
971
appearance of primary and secondary tumors of the liver. Radiology 101:539-548,Dec. 1971. 25. Williams, R.C., Wise, R.E.: Infusion hepatic angiography-assessment of hepatic malignancy via the infusion catheter. Rad. Clinics North Am. 8: 43-51, Apr. 1970. 26. Wirtanen, G.W.: A new angiographic technique in the diagnosis of liver tumors. Radiology 108: 51-54, July 1973. 27. Yu, C.: Primary carcinoma of the Iiver (Hepatoma): its diagnosis by selective celiac arteriography. Am. J. Roentgenol. 99: 142-149, 1%7.
Oncolog~
Biel.
Phys.,
1976. Vol.
1. pp. 965-971.
ANGIOGRAPHY
Pergamon
of Radiology.
Printed
OF HEPATIC A REVIEW
DAVID Department
Pres.
University
G.
in the
U.S.A.
NEOPLASMS:
BRAGG, M.D.
of Utah Medical U.S.A.
Center,
Salt Lake City. UT 84132.
Selective angiographic techniques provide the clinician with another method to evaïuate the Ever for space occupying lesions. Basicahy, tumor vascularity, wen more than size, is the critical factor in the angiographic expression of these mass lesions. The typical hepatoma, solitary and multfnodular forms, usually is visuahzed with ease. More often, scirrhous cholangiocarcinoma is a much more diicult angiographic diagnosis, since less dramatic vascular changes are associated with it. Of the metastatic tumors to the liver, dfffuse adenocarcinoma secondaries from the GI tract are more common, and show iess vivid vascular changes. Since al1 neoplasms of the liver derive their vascuiar supply from hepatic arteries, the late phase of the angiogram or the portogram wil1 show negative filling defects, occasionally as smal1 as 1 cm in size. Since these filling defects are non-spec&, the arteriographic changes subsequent to the tumor must be evahtated carefully to make a specific diagnosis. The arteriographic features of some benign Ever tumors are mentioned, only in a dferential setting, since they usualty can be distinguished from their maiignant counterparts. The exceptfon to this latter statement is the liver cell adenoma which resembles a hepatoma angiographically. Hepatic neoplasms,
PLAIN
FILM
Angiography,
Tumor
vascularity,
PINDINGS
Metastatic
liver disease.
sites reported to be associated with calcified metastatic liver lesions have been ovarian serous cystadenocarcinoma, neuroblastoma, breast and lung carcinomas, and melanoma.’
film of the abdomen plays a small, but occasionally dramatic role in the diagnosis of hepatic neoplasms. In benign lesions, the caverneus hemangioma uncommonly may calcify, usually with amorphous calcium deposits within the fibrous septa of the tumor. It is quite rare to observe phleboliths within Of the primary malignant hemangiomas.” hepatic tumors, the hepatoma most frequently contains sufficient calcium to be visible radiographically, an event more commonly noted in those tumors presenting in childWhen seen, the calcium deposits hood.” appear as a dense, tumoral mass. Of the metastatic hepatic tumors, a number of lesions may be visible on plain films. As a group, the mucin producing adenocarcinomas are said to contain calcium most frequently. They may occur anywhere in the GI tract? but are found most often in the left colon. Other primary
Bierman et aL5 first reported the successful catheterization of the celiac and superior mesenteric arteries in the evaluation of liver disease, together with the angiographic features of liver tumors. After the present technique for selective arterial catheterization was introduced in 1953, hepatic angiography became an acceptable, low risk method for the evaluation of liver abnormalities.4 A discussion of angiographic equipment, techniques, anatomy and complications appears in Stilberg and Bierman.z1 Both primary and metastatic hepatic tumors receive their blood supply from the hepatic
Acknowledgement-The efforts of Dr. P. Ruben
offering many helpful suggestions ment of this review paper.
The
plain
author Koehler
appreciates in reviewing
the and
ANGIOGRAPHIC PROCEDURES TERMINOLOGY
965
AND
in the develop-
966
Radiation Oncology 0 Biology 0 Physics
September-October
arterial tree. Study of the hepatic venous system seldom is of value in the workup of liver neoplasms because the direction of blood flow is away from the liver. Opacification of the portal venous system does have value in this disease setting, both with regard to displacement and involvement of the portal system from the neoplasm as wel1 as in the delineation of the mass lesion as a “negative” filling defect(s) during the portogram phase. Since no tumor derives any significant portion of its blood supply from the portal circulation, the site of the neoplasm always appears as a “negative” defect regardles of etiology. In approximately 50% of cases with known liver space occupying masses, the portogram phase of the angiographic study wil1 reveal their presence.” The threshold size of a lesion for detection is estimated to be 1 cm, but in practice, the lesion must usually be larger to be seen. Tumor vascularity, not size is the critical factor in allowing angiographic diagnosis, as wil1 be explained later. The angiographic approach to the portal venous system now is either by catheterization directly of its tributaries or subsequent to the injection of the splenic or superior mesenteric arterial tree. The more hazardous direct splenic pulp injections have been abandoned largely in favor of these safer catheter approaches. Priscoline injected into the superior mesenteric artery enhances the subsequent portal vein opacification. An understanding of the angiographic patterns of the different primary and metastatic hepatic neoplasms can be complimented with a knowledge of their histopathologie composition. This discussion wil1 focus on the hepatic cel1 type (hepatoma) and the duet cel1 malignant primary (cholangiocarcinoma) eithelial tumors. Although pathologie examples of mixed tumors are reported, the dominant cel1 type largely determines their clinical and angiographic characteristics. The benign hepatic neoplasms wil1 be discussed only in a differential setting. The reader is referred to the bibliography for a more in depth discussion of these entities.“‘.‘5.‘6 To the individual not familiar with angiographic terminology, a brief glossary seems appropriate. “Cuffing” of vessels refers to
1976, Vol. 1, Number 9 and Number 10
irregular narrowing of arteries as a result of tumor encasement. It is more commonly seen in primary tumors but may occur in metastatic lesions as well. Tumor vessels are the angiographic expression of neovascularity. These arteries develop in response to the tumor and are unique physiologically in lacking a smooth muscle cuff capable of responding to vasoconstrictive drugs. This latter feature allows the use of vasoactive agents to enhance the angiographic appearance of a tumor by diminishing or obliterating the non-neoplastic, normal arterial bed. Angiographically tumor vessels are characterized by disorganization. They widen and narrow irregularly and branch in a non-random manner, leading to the formation of irregular contrasts pools or lakes. A “tumor stain” is an abnormality observed during the capillary phase of the angiographic within the study.24 Contrast concentrations tumor capillary bed create a blush which tends to correlate both with the size and vascularity of the primary or metastatic lesion. Arteriovenous shunting refers to early venous filling. It is an infrequently observed angiographic abnormality which, with increased arterial flow, is more commonly seen with primary hepatic cel1 tumors; however it also occasionally may be noted in the presence of metastatic disease to the liver.“.24 “Corkscrew vessels” is the descriptive label given to the appearance of the arterial tree of the end stage cirrhotic liver. It is a non-specific observation, produced by any condition associated with marked contracture of liver volume, of which cirrhosis is, of course, the most common.*.*’ “Draping” of vessels refers to the non-specific displacement of the arteries and veins around a mass lesion (Fig. 1). The first angiographic step in the evaluation of an hepatic mass lesion is the determination of its location within the liver. This may not always be an easy task in spite of the criteria outlined by Rossi and Ruzicka.*’ Extrahepatic mass lesions, on occasion, exactly mimic the appearance of intrahepatic tumors, necessitating the injection of neighboring arteries and requiring the use of additional projections to aid in this differentiation.*’ The purposes of hepatic angiography are not only in establishing the presence and
Angiography
of hepatic neoplasms
0 D. CT. BRAGG
967
The potential communications between the celiac and superior mesenteric systems frequently are recruited in instances of occlusive vascular disease as well. Knowledge of these vascular variations is vita1 to the angiographer as wel1 as the surgeon and oncologist when planning resection or perfusion of hepatic malignancies.
Fig. 1. Patient JS-This 44 year old male presented with a history of amoebic hepatitis diagnosed subsequent to his return from Korea. A positive liver scan led to this angiogram which demonstrates extensive tumor replacement principally involving the right lobe of the liver, but also extending to the left lobe. A discrete mass in the subphrenic area of the liver represents the largest vascular tumor (single arrow t ) with smaller lesions identified by the double arrow ( T T ) in the inferior and lateral margin of the liver as wel1 as centrally in the right lobe. This multicentric lesion is malignant angiographically and felt consistent, either with a multicentric hepatoma or a vascular metastatic lesion such as a carcinoid tumor. At surgery a multifocal hepatoma was found. This tumor characterizes the vivid angiographic alterations of the solitary massive hepatoma and shows examples of tumor vessels and “draping” of vessels.
nature of hepatic mass lesions, but also in defining the extent of involvement and outlining the vascular roadmaps for possible hepatic resection or chemotherapeutic perfusion. It should be recalled that in approximately 16% of cases, the right hepatic artery arises from the superior mesenteric artery. Similarly. there is an 18% incidence of the left hepatic artery arising from the left gastric branch.‘O
PRIMARY LIVER TUMORS YuZ7 has reported a large angiographic series of 50 hepatomas and divided the tumors into three gross patterns: solitary massive (8 cases), nodular (10 cases) and diffuse (32 cases). The most dramatic angiographic patterns were described in the solitary massive and diffuse forms (increased vascularity, tumor vessels, tumor stain, A-V shunting). Dilation of the hepatic artery was noted in al1 50 cases, presumably as a reflection of the increased vascular demand by the tumor. Using a different approach, Kido, Sasaki and Kaneko13 correlated the histologie types of the primary malignant hepatic epithelial tumors with their angiographic characteristics. In the wel1 differentiated hepatomas (24 cases), al1 showed tumor vessels, with the majority revealing both tumor stains and A-V shunting (19 of 24 and 17 of 24 respectively). Of the anaplastic hepatomas (six cases). tumor vessels and tumor stains were noted in four and A-V shunting in one. Of the seven cholangiocarcinomas, tumor vessels and tumor staining characterized four, however, none were noted to have A-V shunting. The angiographic similarity between anaplastic hepatomas and cholangiocarcinomas is suggested by these observations. Using the above defined criteria of Yu, Gammill et al.’ proposed an angiographic scheme useful in predicting the aggressiveness and extent of the primary hepatic tumor and the chances of its being respectable surgically. They suggest a chronologie trend in the evolution of angiographic changes in a malignant epithelial type hepatic tumor, from first developing tumor neovascularity, tumor blood pooling, then tumor staining and finally becoming avascular as the tumor outgrows its blood SUPPlY.
968
Radiation
Oncology
??Biology 0 Physics
September-October
1976, Vol. 1, Number 9 and Number
10
(bl (al
Figs. 2(a-c). An axillary selective right hepatic arterial injection shows a centra1 large mass lesion in the right lobe of the liver with vessels “draped” around the lesion (2a) throughout. The hepatogram phase (2b) demonstrates diffuse “tumor stains” irregularly throughout the right lobe of the liver (arrows). The transverse ultrasound scan (2~). B mode demonstrates the abnormal return echoes within the substance of the liver defining the largest of the space occupying lesion (arrows) solid by sonographic characteristics. The diagnosis was metastatic tumor from a primary in the colon, showing the vascular nature of these lesions similar to the multifocal hepatoma shown in Fig. 1. In contrast to the hepatic cel1 tumor, the bile duet primary tumors tend to be scirrhous in form, more invasive, with less of a mass and usually unimpressive tumor effect, These bile duet neoplasms neovascularity.6.iZ are quite obviously a greater angiographic challenge in diagnosis. Arterial encasement or rather than displacement or obstruction, “draping” is reported in 81%; the reverse is true with hepatomas. As cholangiocarcinomas arise most frequently near the junction of the
cystic and common ducts, a careful review of the angiogram may show smal1 beaded tumor vessels in the region of the liver hilus. In spite of the centra1 origin of cholangiocarcinomas, adjacent to the portal vein, this venous trunk seldom is involved by the tumor, yet commonly is obstructed with hepatomas (portal vein abnormalities are reported in 13% of cholangiocarcinomas in contrast to 45% of hepatomas.” An angiographic analogy exists with the primary renal tumors which is similar
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lasia and regenerating liver nodules in cirrhoto the cholangiocarcinoma: hepatoma model in the transitional cell: hypernephroma ar- tic patients, the scan serves as a diagnostic complement to the angiogram.7.‘6 teriographic patterns of presentation. The size threshold for the recognition of a Carcinoma of the gallbladder has proven to is smaller than be the diagnostic enigma with reference to the mass lesion angiographically the reported 2 cm lesion in the radionuclide biliary tree. The uncommon epidermoid form hepatogram; occasionally, it may approach of this tumor should provide a better arteriographic model; however, an adenocarcinoma is 1 cm. The vascularity of the primary tumor the more common histologie type. and it determines the angiographic expression of the usually presents in a scirrhous pattern, further metastatic lesions. Visualization also depends on the location of the lesion within the liver, limiting the angiographer’s ability to recognize gallbladder cancer. However, Abrams el al.’ as we11 as the extent of involvement present. Of the vascular metastatic hepatic lesions, the were able to diagnose correctly 6 cases following are included: hypernephromas, by selective celiac and superior mesenteric lieomyosarcomas, carcinoid tumors, islet cell angiography. In each example, the cystic and papillary cell tumors of the pancreas, and artery was enlarged with cuffing or amputation transitional cel1 tumors. Of the avascular of one of its branches. In addition, the angiographic metastatic lesions, adenocarabnormal tumor stain created a thick. uneven cinomas lead the list, specifically those of the gallbladder wal], feit to be specific for tumor. pancreas, and breast. Primary Extension to the liver from the primary site in stomach, tumors of the lung, adrenal gland and the gallbladder created an abnormal vascular melanoma also should be mentioned.‘b”’ pattern at the involved site. NO false positive Metastatic lesions have been reported to or negative examples were reported. In summary, the angiographer’s ability to mimic all of the angiographic changes of diagnose primary malignant hepatic tumors primary liver tumors. At the other extreme is the group of avascular metastatic lesions depends upon the degree of vascularity induced by the tumor. This can vary from described above which may show only an uneven hepatogram which of itself, is quite dramatic in the case of the solitary massive non-specific.* Other angiographic signs of hepatoma, to the very subtle or non-existent tumor must be visualized, particularly with angiographic changes with the cholangiocardiffuse metastatic disease, to be confident of cinema and gallbladder tumors. the diagnosis. METASTATIC LIVER DISEASE Of the benign hepatic neoplasms, the With regard to metastatic disease to the caverneus hemangioma is the most important liver, the angiographer must be concerned to recognize. This mass lesion may be single with his accuracy in the recognition of or multiple, large or smal], presenting with secondary tumors as we11 as his ability to impressively abnormal, increased vascularity. NO true tumor vessels or evidente for distinguish these lesions from primary maligvascular cuffing occurs with benign lesions. nant and benign hepatic lesions. Angiography clearly carries too great a risk and tost to be The delayed angiographic films reveal the diagnostic features of a caverneus hemanuseful as a routine screening procedure for the detection of metastatic disease.* The quoted gioma: late (lg-20 sec) pooling of contrast in angiographic accuracy approaches that of sinusoidal lakes found within these masses. radionuclide liver scanning in the detection of Their recognition is important as blind needle biopsy of these vascular lesions may be hepatic mass lesions, but is more specific.‘*.” Superselective and magnification angiographic disastrous.“.” Examples of f&al nodular hyperplasia of techniques as wel1 as pharmacologic aides the liver are said to show suficient angioghave improved this accuracy in recent years. At present, angiography serves as a means of raphic differences to allow their distinction from malignant tumors. These diff erences evaluation of the non-specific, abnormal relate to the feeding arteries which arise from radionuclide scan. With focal nodular hyperp-
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the periphery of the tumor, together with the absente of true tumor vessels, A-V shunting and portal vein invo1vement.7.‘0.‘6 Nuclear scanning in focal nodular hyperplasia wil1 fail to show a mass lesion, confirming the diagnosis. The angiographic features of liver cel1 adenoma usually are undistinguishable from those of a hepatoma. Infusion techniques have been introduced in an attempt to enhance the screening accuracy of the hepatic angiogram in the detection of mass lesions. This method is reported to allow for an improved accuracy in the diagnosis of mass lesions, but obviates the more specific means to recognize the arteriographic criteria of malignant hepatic primaries.25.26 In recent years, improvement in ultrasound imaging potential has provided yet another means of iiver imaging. This modality serves to compliment the above described angiog-
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raphic techniques, particularly with regard to the differentiation of cystic from solid tumor masses. In summary, hepatic arteriography has enhanced significantly the clinician’s ability to diagnose accurately and manage the patient with a mass lesion of the liver. As experience in this field has developed, both the limitations and the need for exquisite technique and film quality has been magnified. In perspective, the hepatic angiogram is the major diagnostic procedure in the pre-treatment evaluation of the patient suspected of having a primary liver tumor both with respect to the pre-biopsy localization and the pre-surgical definition. Although many benign and metastatic liver masses may have significant vascular abnormalities allowing their angiographic recognition, considerable experience and ski11 is required to specifically categorize and define them.
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Bookstein, J.J., Appelman, H.D.: Angiographic findings in benign liver cel1 tumors. Radiology
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110: 339-343, Feb. 1974. 11. Jewel, K.L.: Primary carcinoma of the liver: clinical and radiologie manifestations. Am. J. Roentgenol. 113: 84-91, Sept. 1971. 12. Kaude, J., Rian, R.: Cholangiocarcinoma. Radiology 100: 573-580, Sept. 1971. 13. Kido, C., Sasaki, T., Kaneko, M.: Angiography of primary liver cancer. Am. J. Roentgenof. 113: 70-81, Sept. 1971. 14. McDonald, P.: Hepatic tumours in childhood. Clin. Radiol. 18: 74-82, 1%7. 15. McLoughlin, M.J.: Angiography in caverneus hemangioma of the liver. Am. J. Roentgenol. 113: 50-55, 1971. 16. McLoughlin, M.J., Colapinto, R.F., Gilday, D.L., Hobbs, B.B., Korobkin, M.T., McDonald, P., Phillips, M.J.: Focal nodular hyperplasia of the liver: angiography and radioisotope scanning. Radiology 107: 257-263, May 1973. 17. Mess, A.A., Clark, R.E., Palubinskas, A.J., DeLorimier, A.A.: Angiographic appearance of benign and malignant hepatic tumors in infants and children. Am. J. Roentgenol. 113: 61-69, 1971. 18. Nebesar, R.A., Pollard, J.J., Stone, D.L.: Angiographic diagnosis of malignant disease of the liver. Radiology 86: 284-292, 1%6. 19. Pollard, J.J., Fleischli. D.J., Nebesar, R.A.: Angiography of hepatic neoplasms. Rad. Clinics North Am. 8: 3141, Apr. 1970. 20. Pollard, J.J., Nebesar, R.A.: Abdominal angiog-
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appearance of primary and secondary tumors of the liver. Radiology 101:539-548,Dec. 1971. 25. Williams, R.C., Wise, R.E.: Infusion hepatic angiography-assessment of hepatic malignancy via the infusion catheter. Rad. Clinics North Am. 8: 43-51, Apr. 1970. 26. Wirtanen, G.W.: A new angiographic technique in the diagnosis of liver tumors. Radiology 108: 51-54, July 1973. 27. Yu, C.: Primary carcinoma of the Iiver (Hepatoma): its diagnosis by selective celiac arteriography. Am. J. Roentgenol. 99: 142-149, 1%7.