Published online before print June 28, 2002, 10.1148/radiol.2242011283
(Radiology 2002;224:542-547.)
© RSNA, 2002
Vascular and Interventional Radiology |
Variant Hepatic Arterial Anatomy Revisited: Digital Subtraction Angiography Performed in 600 Patients1
Anne M. Covey, MD,
Lynn A. Brody, MD,
Mary A. Maluccio, MD, MPH,
George I. Getrajdman, MD and
Karen T. Brown, MD
1 From the Department of Diagnostic Radiology, Memorial Sloan-Kettering Cancer Center, 1275 York Ave, New York, NY 10021 (A.M.C., L.A.B., G.I.G., K.T.B.); and Department of Surgery, New York Presbyterian Hospital, New York, NY (M.A.M.). Received July 26, 2001; revision requested September 4; revision received October 23; accepted December 11. Address correspondence to A.M.C. (e-mail: coveya@mskcc.org).
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ABSTRACT
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PURPOSE: To evaluate and describe the prevalence of hepatic arterial variants seen at digital subtraction angiography in a large series of patients.
MATERIALS AND METHODS: Data were collected prospectively by using an arterial anatomy database questionnaire that was completed at the time each visceral angiographic examination was performed from May 1996 to October 2000.
RESULTS: Six hundred patients underwent at least one visceral angiographic examination at one institution during the study period. Three hundred sixty-eight (61.3%) patients had the standard hepatic arterial anatomy. One hundred nineteen (19.8%) patients had variant left hepatic arteries (LHAs), and 89 (14.8%) had variant right hepatic arteries (RHAs). Twenty-eight (4.7%) patients had a variant anatomy involving both the LHA and the RHA. Twenty-four (4.0%) patients had a variant origin of the common hepatic artery (CHA) arising from either the superior mesenteric artery (SMA) or the aorta. In two patients, the proper hepatic artery (PHA) was the first branch of the SMA and the gastroduodenal artery (GDA) was a branch of the celiac axis. Double hepatic arteries were seen in 22 (3.7%) patients. Trifurcation or quadrifurcation of the GDA was seen in 50 (8.3%) patients, and the GDA originated distal to one hepatic artery in 25 (4.2%) patients in whom both hepatic arteries originated from the CHA.
CONCLUSION: A replaced LHA was less common than has been previously reported, and in two cases, the PHA arose from the SMA. Digital subtraction visceral angiographic results are comparable to results of seminal angiographic studies in which the cut-film technique was used.
© RSNA, 2002
Index terms: Angiography, 952.122 • Hepatic arteries, 952.132, 952.92
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INTRODUCTION
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In his 1955 text, Michels (1) described his classification scheme for describing anatomic variation in the hepatic arterial blood supply based on the results of dissecting 200 cadavers. In 1969, Vandamme et al (2) published their experiences with 156 postmortem angiograms that were obtained before anatomic dissection. Then, in 1971, Suzuki et al (3) contributed an article on the surgical importance of anatomic variants of the hepatic arteries that was based on findings in 200 patients who were examined with cut-film angiography.
In the 3 decades since the publication of these seminal articles, major technical advances in angiography have occurred; these include the advent of digital subtraction angiography (DSA), which has virtually replaced cut-film angiography for most applications in the United States. The interventional and surgical options for patients with primary and metastatic liver tumors also have expanded dramatically during this period. Now more than ever surgeons and interventional radiologists are relying on accurate imaging and assessment of the hepatic arterial supply.
The purpose of this study was to evaluate and describe the prevalence of the hepatic arterial variants seen with DSA in a large series of patients.
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MATERIALS AND METHODS
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From May 1996 to October 2000, the hepatic arterial anatomy of all patients who underwent visceral angiography at the Memorial Sloan-Kettering Cancer Center was reviewed. Preoperatively, patients were examined angiographically most commonly for assessment for placement of a hepatic arterial infusion pump that was used to administer intraarterial chemotherapeutic agents or when computed tomographic (CT) arterial portography was performed. Data were also collected from patients who underwent hepatic arterial embolization for the treatment of primary or metastatic liver tumors. At the time this study began, our institutional review board did not require its approval; however, informed consent was obtained from all patients.
The only inclusion criterion was having undergone visceral angiography, including that of all normal branches of the celiac axis and the superior mesenteric artery (SMA). Attempts were made to image the left gastric artery (LGA) in all patients. Patients who previously had undergone hepatic resection were excluded. Duplicate data on individual patients, such as those who were undergoing repeat embolization, were not included.
All angiographic examinations were performed by one of six fellowship-trained interventional radiologists (A.M.C., L.A.B., K.T.B., G.I.G.). Data were recorded on a standard form immediately following angiography and entered into an electronic database by one author (A.M.C.). The common hepatic artery (CHA), SMA, proper hepatic artery (PHA), gastroduodenal artery (GDA), left hepatic artery (LHA), and right hepatic artery (RHA) each had to be categorized as standard, accessory, replaced (ie, case in which the entire arterial blood supply to a side of the liver arises from an atypical location), or "other" on the form. Accessory or replaced vessels were further categorized according to the vessel from which they originated, and a categorization of other was accompanied by a labeled drawing on the form.
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RESULTS
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During the study period, 629 patients underwent visceral angiography, but 11 were excluded from the study because the data form was incomplete and the images were not available for review. An additional 18 patients with surgically removed hepatic or gastroduodenal arteries also were excluded. Therefore, 600 visceral angiograms obtained in 600 patients were available for review (Table). The indication for angiography was preoperative planning in 344 patients, hepatic arterial embolization in 235, hepatic chemotherapeutic agent infusion in 10, gastrointestinal bleeding in five, splenic artery embolization in two, infusion of gene therapy in two, localization of insulinoma in one, and unknown in one.
Three hundred sixty-eight patients (61.3%) had the standard hepatic arterial anatomy (Fig 1). We included patients with a variant origin of only the GDA in this group for purposes of comparison with findings in previously published series. The presence or absence of a middle hepatic artery also was considered normal. In 73 (12.2%) patients the RHA was replaced to the SMA (Fig 2), whereas in one patient the RHA was replaced to the right phrenic artery. In 27 (4.5%) patients the LHA was replaced to the LGA (Fig 3).
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Figure 1. Anteroposterior angiogram of standard hepatic arterial anatomy. The celiac axis gives rise to the LGA (small short arrow), splenic artery (open arrow), and CHA (long straight arrow). After the origin of the GDA (arrowhead), the CHA becomes the PHA (curved arrow). The PHA bifurcates into the RHA (large short arrow) and LHA (thin arrow).
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Figure 2a. Anteroposterior angiograms show RHA replaced to SMA. (a) Angiogram of the celiac axis shows CHA (straight arrow) bifurcating into the GDA (arrowhead) and the LHA (curved arrow). No RHA is depicted. (b) After injection of contrast material into the SMA (open arrow), the angiogram shows a replaced RHA (solid arrow).
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Figure 2b. Anteroposterior angiograms show RHA replaced to SMA. (a) Angiogram of the celiac axis shows CHA (straight arrow) bifurcating into the GDA (arrowhead) and the LHA (curved arrow). No RHA is depicted. (b) After injection of contrast material into the SMA (open arrow), the angiogram shows a replaced RHA (solid arrow).
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Figure 3. Anteroposterior angiogram shows LHA replaced to LGA. Angiogram of the celiac axis (not shown) demonstrated the RHA arising from the CHA. No LHA was visualized. After injection of contrast material into the gastrolienal artery, this angiogram shows the LHA (curved arrow) originating from the LGA (straight solid arrow). The splenic artery is identified by the open arrow.
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Accessory RHAs were seen in 15 (2.5%) patients: 11 accessory RHAs originated from the SMA (Fig 4a, 4b), and one each originated from the GDA (Fig 4c), LGA (Fig 4d, 4e), celiac axis, and right phrenic artery.
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Figure 4a. Anteroposterior angiograms show accessory RHAs. Angiograms of the (a) celiac axis and (b) SMA show the RHA (curved arrow in a) at the normal site and an accessory RHA (curved arrow in b) arising from the SMA (straight arrow in b), the most common site for accessory RHAs. The LHA (small arrow in a) and CHA (large straight arrow in a) are normal. (c) Angiogram shows the uncommon case of an accessory RHA (curved white arrow) arising from the GDA (arrowhead). The RHA at the normal site is identified by the curved black arrow. (d) Angiogram of the celiac axis shows the CHA (straight arrow), RHA (curved black arrow), and LHA (white arrow). (e) Angiogram obtained in the same patient as in d shows the single case of an accessory RHA (curved black arrow) arising from the LGA (straight arrow). The accessory RHA also gives rise to an accessory LHA (white arrow).
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Figure 4b. Anteroposterior angiograms show accessory RHAs. Angiograms of the (a) celiac axis and (b) SMA show the RHA (curved arrow in a) at the normal site and an accessory RHA (curved arrow in b) arising from the SMA (straight arrow in b), the most common site for accessory RHAs. The LHA (small arrow in a) and CHA (large straight arrow in a) are normal. (c) Angiogram shows the uncommon case of an accessory RHA (curved white arrow) arising from the GDA (arrowhead). The RHA at the normal site is identified by the curved black arrow. (d) Angiogram of the celiac axis shows the CHA (straight arrow), RHA (curved black arrow), and LHA (white arrow). (e) Angiogram obtained in the same patient as in d shows the single case of an accessory RHA (curved black arrow) arising from the LGA (straight arrow). The accessory RHA also gives rise to an accessory LHA (white arrow).
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Figure 4c. Anteroposterior angiograms show accessory RHAs. Angiograms of the (a) celiac axis and (b) SMA show the RHA (curved arrow in a) at the normal site and an accessory RHA (curved arrow in b) arising from the SMA (straight arrow in b), the most common site for accessory RHAs. The LHA (small arrow in a) and CHA (large straight arrow in a) are normal. (c) Angiogram shows the uncommon case of an accessory RHA (curved white arrow) arising from the GDA (arrowhead). The RHA at the normal site is identified by the curved black arrow. (d) Angiogram of the celiac axis shows the CHA (straight arrow), RHA (curved black arrow), and LHA (white arrow). (e) Angiogram obtained in the same patient as in d shows the single case of an accessory RHA (curved black arrow) arising from the LGA (straight arrow). The accessory RHA also gives rise to an accessory LHA (white arrow).
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Figure 4d. Anteroposterior angiograms show accessory RHAs. Angiograms of the (a) celiac axis and (b) SMA show the RHA (curved arrow in a) at the normal site and an accessory RHA (curved arrow in b) arising from the SMA (straight arrow in b), the most common site for accessory RHAs. The LHA (small arrow in a) and CHA (large straight arrow in a) are normal. (c) Angiogram shows the uncommon case of an accessory RHA (curved white arrow) arising from the GDA (arrowhead). The RHA at the normal site is identified by the curved black arrow. (d) Angiogram of the celiac axis shows the CHA (straight arrow), RHA (curved black arrow), and LHA (white arrow). (e) Angiogram obtained in the same patient as in d shows the single case of an accessory RHA (curved black arrow) arising from the LGA (straight arrow). The accessory RHA also gives rise to an accessory LHA (white arrow).
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Figure 4e. Anteroposterior angiograms show accessory RHAs. Angiograms of the (a) celiac axis and (b) SMA show the RHA (curved arrow in a) at the normal site and an accessory RHA (curved arrow in b) arising from the SMA (straight arrow in b), the most common site for accessory RHAs. The LHA (small arrow in a) and CHA (large straight arrow in a) are normal. (c) Angiogram shows the uncommon case of an accessory RHA (curved white arrow) arising from the GDA (arrowhead). The RHA at the normal site is identified by the curved black arrow. (d) Angiogram of the celiac axis shows the CHA (straight arrow), RHA (curved black arrow), and LHA (white arrow). (e) Angiogram obtained in the same patient as in d shows the single case of an accessory RHA (curved black arrow) arising from the LGA (straight arrow). The accessory RHA also gives rise to an accessory LHA (white arrow).
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An accessory LHA almost always arose from the LGA (Fig 5), as was seen in 90 patients in our series. In two patients, the accessory LHA arose from other sources, including the anterior division of the RHA. In one case, an accessory LHA arose from an accessory RHA off the LGA (Fig 4d, 4e). Six patients (1.0%) in our series had both an accessory RHA and an accessory LHA, and 19 patients (3.2%) had a replaced RHA or LHA associated with an accessory LHA or RHA.
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Figure 5. Anteroposterior angiogram of celiac axis shows an accessory LHA. Accessory LHAs (curved white arrow) almost exclusively originate from the LGA (straight arrow), as shown here. The other LHA is indicated by the curved black arrow.
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A variant origin of the CHA was seen in 24 (4.0%) patients in our series. In 12 (2.0%) patients the CHA was replaced to the SMA (Fig 6), and in another 12 the CHA arose as a separate branch of the aorta (Fig 7).
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Figure 6. Anteroposterior angiogram shows CHA replaced to the SMA. Four percent of the patients in this series had an anomalous origin of the CHA. In half of these patients, the CHA (straight solid arrow) was replaced to the SMA (open arrow), as in this case. The RHA (arrowhead) and LHA (curved arrow) are normal.
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Figure 7a. Separate origin CHA and gastrolienal trunk. In 50% of cases in which there is a variant origin of the CHA, the CHA arises as a separate branch of the aorta. (a) Anteroposterior angiogram of the CHA arising directly from the aorta (arrow). (b) Anteroposterior angiogram of a gastrolienal artery (arrow) that arises as a separate branch of the aorta.
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Figure 7b. Separate origin CHA and gastrolienal trunk. In 50% of cases in which there is a variant origin of the CHA, the CHA arises as a separate branch of the aorta. (a) Anteroposterior angiogram of the CHA arising directly from the aorta (arrow). (b) Anteroposterior angiogram of a gastrolienal artery (arrow) that arises as a separate branch of the aorta.
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Variant anatomy of the PHA is quite rare. In two patients (0.3%) this vessel was replaced to the SMA and the GDA originated as a separate branch of the aorta (Fig 8).
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Figure 8a. Anteroposterior angiograms show PHA replaced to the SMA. (a) Angiogram of celiac axis shows the LGA (solid arrow), splenic artery (open arrow), and GDA (arrowhead). No hepatic artery is depicted. (b) Angiogram of SMA region shows a replaced PHA (straight solid arrow) as the first branch of the SMA (open arrow). The PHA gives rise to the LHA (curved arrow) and the RHA (arrowhead).
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Figure 8b. Anteroposterior angiograms show PHA replaced to the SMA. (a) Angiogram of celiac axis shows the LGA (solid arrow), splenic artery (open arrow), and GDA (arrowhead). No hepatic artery is depicted. (b) Angiogram of SMA region shows a replaced PHA (straight solid arrow) as the first branch of the SMA (open arrow). The PHA gives rise to the LHA (curved arrow) and the RHA (arrowhead).
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Another uncommon but important variant that is not included in the Michels classification is the so-called double hepatic artery (4), which refers to a case in which one or both hepatic arteries originate from either the celiac axis directly or the aorta. Double hepatic artery is differentiated from distal, or "late," origin of the GDA by the presence of a CHA. In the case of a double hepatic artery, there is no CHA and the GDA may originate from either hepatic artery. In the case of a distal origin of the GDA, the GDA originates from one hepatic artery after the division of the CHA into the RHA and LHA. Twenty-five (4.2%) patients had late origin of the GDA (Fig 9). In 22 (3.7%) patients the GDA arose from the RHA, and in the other three (0.5%) patients it arose from the LHA. Twenty-two (3.7%) patients in our series had double hepatic arteries: In fifteen (2.5%) patients this was due to early branching of the RHA and/or LHA off the celiac axis (Fig 10), and in seven (1.2%) patients one or both hepatic arteries arose directly from the aorta.
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Figure 9. Anteroposterior angiogram shows late origin of the GDA. In 25 of 600 patients in the current study, the GDA arose distal to the origin of one hepatic artery. In the case shown, the GDA (arrowhead) arises just distal to the LHA (curved arrow), which is the first branch of the CHA (straight arrow).
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Figure 10. Anteroposterior angiogram shows a double hepatic artery. In the so-called double hepatic artery, there is no CHA and the GDA may originate from either hepatic artery. In the case shown, the RHA (straight solid arrow) and LHA (curved arrow) arise separately from the celiac axis. The GDA (arrowhead) originates from the LHA. The splenic artery is indicated by the open arrow.
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Trifurcation of the CHA into the GDA, RHA, and LHA, although not considered a variant by most authors (3,5,10), does have important surgical relevance, particularly for patients who are having pumps placed for hepatic arterial infusion of chemotherapeutic agents. Trifurcation occurred in 50 patients (8.3%) in our series (Fig 11a); this is more frequent than the 2.0% of patients in whom this occurred in the study of Vandamme et al (2). Three (0.5%) patients had quadrifurcation of the CHA into the GDA, RHA, LHA, and middle hepatic artery (Fig 11b).
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Figure 11a. Anteroposterior angiograms show variant origins of the GDA. (a) Trifurcation of the CHA into the LHA (curved arrow), RHA (open arrow), and GDA (arrowhead). (b) Quadrifurcation of the CHA (large straight solid arrow) into the LHA (curved arrow), RHA (open arrow), middle hepatic artery (small straight solid arrow), and GDA (arrowhead). These anomalies often are not included in the classic anatomy literature, but they have important implications in interventional and surgical procedures.
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Figure 11b. Anteroposterior angiograms show variant origins of the GDA. (a) Trifurcation of the CHA into the LHA (curved arrow), RHA (open arrow), and GDA (arrowhead). (b) Quadrifurcation of the CHA (large straight solid arrow) into the LHA (curved arrow), RHA (open arrow), middle hepatic artery (small straight solid arrow), and GDA (arrowhead). These anomalies often are not included in the classic anatomy literature, but they have important implications in interventional and surgical procedures.
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The LGA was visualized in 583 (97.2%) patients. Three LGA variants were seen: a separate origin from the aorta in 21 (3.5%) patients, a gastrolienal trunk in 12 (2.0%) patients, and a gastrophrenic trunk in six (1.0%) patients.
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DISCUSSION
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In the standard, or classic, visceral anatomy, the celiac axis gives rise to three branches (5). The first branch is the LGA, after which the vessel divides into the splenic artery and CHA. The CHA then bifurcates into the GDA and PHA, and the PHA bifurcates into the RHA and LHA.
Standard hepatic arterial anatomy has been reported in approximately 50% of patients on the basis of cadaveric and early angiographic reports (1–3,15–17). In 1969, Redman and Reuter (6) reported in a frequently referenced article that "most of the variations of the other 50% have little surgical significance." Because of the advent of interventional and surgical techniques to treat both primary and metastatic liver tumors (7,8) and the increasing availability of living related liver transplant donors, the accurate depiction and definition of the hepatic arterial anatomy are crucial. It is important that interventional radiologists who perform hepatic arterial embolization be familiar with both common and rare hepatic arterial variants, because failure to recognize the presence of an aberrant vessel can result in incomplete embolization of liver tumors. Familiarity with these variants can also help one avoid various surgical complications.
Several authors (4,18) have proposed that the word aberrant rather than accessory be used to describe cases in which one branch that is supplying blood to one side of the liver arises ectopically and the remainder of the supply is from the typical location, because such branches almost invariably supply a distinct territory of one side of the liver. Although some use the terms aberrant and accessory interchangeably, it is recognized that the word accessory is often a misnomer in these cases, even though it is the more frequently used descriptive term. The term replaced is used to refer to cases in which the entire arterial blood supply to a side of the liver arises from an atypical location.
CT angiography (9,20,21) and gadolinium-enhanced magnetic resonance (MR) angiography (10,11,22,23) are used commonly to assess the visceral anatomy preoperatively. Therefore, it is important that abdominal imagers be familiar with the full gamut of possible hepatic arterial variants. Although the sensitivities of CT angiography and MR angiography for the depiction of hepatic arterial variants are reported in several articles (9–11), in general, the variants in these studies are limited to those described by Michels (1). Our data include important variants that not only interventional radiologists who interpret conventional angiograms but also any radiologist who performs CT angiography or MR angiography should be able to recognize.
Additional clinically relevant anatomic variants that, to our knowledge, have not been described by using CT angiography or MR angiography include double hepatic arteries, replaced or accessory RHAs and LHAs from vessels other than the SMA or LGA, and the unusual situation in which the PHA is replaced to the SMA and the GDA originates from the aorta. To our knowledge, these latter findings have not been described in the radiology literature. Vandamme and Bonte (5) have reported the uniform origin of the GDA from the CHA at the peritoneal reflection that occurs at the junction of the first and second portions of the duodenum.
In a study from the University of Iowa (12), there was good correlation between MR angiography and DSA in the depiction of the degree and length of stenoses in iliac and peripheral vascular disease, but accuracy in the depiction of visceral arteries was lower. Zeh et al (10) described their experiences evaluating hepatic arterial variants in 27 patients who underwent MR angiography for preoperative planning for hepatic arterial infusion pump placement. In their study, 17 patients underwent both MR angiography and DSA. MR angiography enabled the correct identification of all 14 patients with standard anatomy and of three with replaced RHAs. In addition, six accessory LHAs were identified at MR angiography; five of these were confirmed at DSA.
To our knowledge, the largest related series in the MR literature is that from Hamburg, Germany (11); MR angiography was compared with DSA in 60 patients. In that series, MR angiography correctly depicted the visceral arterial anatomy in 57 (95%) cases. Again, it should be noted that although the results of these studies are encouraging, the variants reported in them were limited to those described by Michels (1).
The double hepatic artery, which is not included in the Michels classification, has particular relevance for patients who are being evaluated for hepatic arterial infusion and/or hepatic arterial infusion pump placement. When placed surgically, these catheters are typically placed in the GDA in a retrograde direction with the catheter tip in the proximal GDA or in the PHA. The GDA distal to the catheter insertion site and the right gastric artery and branches supplying blood to the stomach and duodenum are ligated to prevent nontarget infusion (17). In this position, the catheter perfuses the RHA and LHA in a patient with standard anatomy. When placed percutaneously, catheters are typically positioned in the PHA to infuse both hepatic arteries. In cases of a double hepatic artery and of trifurcation or quadrifurcation of the CHA, an alternate catheter position or more than one catheter must be considered preoperatively to ensure adequate tumor perfusion (17,19).
In conclusion, visceral angiography is a critical part of the preoperative evaluation for some hepatobiliary surgeries and many interventional procedures. The DSA findings in this study were similar to those with cut-film angiography observed by Redman and Reuter (6) and to those in cadaveric studies observed by Michels (1). In our opinion, to avoid potentially disastrous complications, one must have a detailed understanding of common and uncommon hepatic arterial variants.
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FOOTNOTES
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Abbreviations: CHA = common hepatic artery,
DSA = digital subtraction angiography,
GDA = gastroduodenal artery,
LGA = left gastric artery,
LHA = left hepatic artery,
PHA = proper hepatic artery,
RHA = right hepatic artery,
SMA = superior mesenteric artery
Author contributions: Guarantor of integrity of entire study, A.M.C.; study concepts and design, A.M.C., K.T.B.; literature research, A.M.C.; clinical studies, A.M.C., G.I.G., L.A.B., K.T.B.; data acquisition, A.M.C., K.T.B., G.I.G., L.A.B.; data analysis/interpretation, A.M.C., M.A.M.; statistical analysis, A.M.C.; manuscript preparation, M.A.M., A.M.C., L.A.B., K.T.B.; manuscript definition of intellectual content, A.M.C.; manuscript editing, K.T.B., L.A.B.; manuscript revision/review, L.A.B., G.I.G., K.T.B.; manuscript final version approval, K.T.B.
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ABSTRACT
INTRODUCTION
