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Right hepatic artery originated from the superior mesenteric artery: What is the standard anatomic position?

ABSTRACT

Objective:

Liver arterial irrigation is characterized by a high frequency of variations in its anatomy. The aim of the study was to describe the anatomic position of the right hepatic artery as a brunch of the superior mesenteric artery.

Methods:

A total of 5147 intravenous contrast-enhanced computed tomography scans of patients seen at the Radiology Service of the Passo Fundo Clinical Hospital (RS), from October 2016 to December 2017, were selected. 125 patients with anatomic variation of the right hepatic artery were selected. The findings were categorized by the variation of the vascular position, emergence from the superior mesenteric artery and the relationship with other structures.

Results:

The most frequent position was retropancreatic (88.8%), retroportal (76.8%) and post-choledocian (75.2%), emerging about 2.33 cm from the superior mesenteric artery.

Conclusion:

We have shown that most common variant of the right hepatic artery presents its posterior origin from the pancreatic and hepatic pedicle, and arises close to the origin of the superior mesenteric artery.

Headings:
Anatomy; Liver; Hepatic Artery

RESUMO

Objetivos:

A irrigação arterial hepática tem como característica a elevada frequência de variações da anatomia. O objetivo do estudo foi descrever o trajeto anatômico da artéria hepática direita quando originada da artéria mesentérica superior.

Métodos:

Foram analisadas 5147 tomografias computadorizadas com contraste endovenoso de pacientes atendidos no Serviço de Radiologia do Hospital de Clínicas de Passo Fundo - RS, no período outubro de 2016 a dezembro de 2017. Foram selecionados 125 pacientes portadores de variação anatômica da artéria hepática direita na origem. Os achados foram categorizados pela variação do trajeto vascular, emergência da artéria mesentérica superior e a relação com demais estruturas.

Resultados:

Obtivemos o trajeto mais frequente desta variação como retropancreático (88,8%), retroportal (76,8%) e pós-coledociano (75,2%), emergindo cerca de 2,33 cm da origem da artéria mesentérica superior.

Conclusão:

Demonstramos que na maioria das vezes, a artéria hepática direita variante, apresenta trajeto posterior ao pâncreas e ao pedículo hepático e emerge próxima da origem da artéria mesentérica superior.

Descritores:
Fígado; Anatomia; Artéria Hepática

INTRODUCTION

According to the anatomists Testut, Moore, Sobotta, and Netter, the most common right hepatic artery anatomic position is as a brunch of the celiac trunk which arises from the aorta. The aorta is the origin of the left gastric artery, splenic artery, and common hepatic artery. The latter is the origin of the gastroduodenal artery and the proper hepatic artery, which is divided into the right and left hepatic arteries, in the hepatic hilum11 Araujo Neto SA, Franca HA, Mello Júnior CF, Silva Neto EJ, Negromonte GRP, Duarte CMA, et al. Anatomical variations of the celiac trunk and hepatic arterial system: an analysis using multidetector computed tomography angiography. Radiol Bras. 2015;48(6):358-62.. However, variations in the hepatic arterial supply may be seen in 25% to 42% of the cases. Therefore, considering the various common hepatic artery anatomy, it is of utmost importance to be aware of its variations since these may impact procedures in the region. A significant number of complications can be prevented while performing any hepatobiliopancreatic procedure22 Fonseca-Neto OCLD, Lima HCS, Rabelo P, Melo PSV, Amorim AG, Lacerda CM. Anatomic variations of hepatic artery: a study in 479 liver transplantations. ABCD Arq Bras Cir Dig. 2017;30(1):35-7..

Thus, we aimed to describe the Right Hepatic Artery (RHA) anatomical position when arising from the superior mesenteric artery (SMA).

METHODS

The study was approved by the Research Ethics Committee of the Federal University of Fronteira Sul under the number 2,851,249 / 2018 and with a waiver for the informed consent. We retrospectively reviewed 5,147 electronic medical records and abdominal Computed Tomography scans (CT) at the Hospital de Clínicas de Passo Fundo - RS, from October 2016 to December 2017. The data were entered twice in the database in the Epidata Software (3.1). The statistical analyses were performed by SPSS Statistics 20.0 (IBM, United States). Quantitative variables were presented as mean ± standard deviation and qualitative variables as frequency and percentage. We did not perform any statistical analysis hypothesis tests.

The CTs were performed by 16-channel or 80-channel multiple detector CT scanners (both Aquilion, Toshiba Medical Systems, Tokyo, Japan), with intravenous injection of non-ionic water-soluble iodinated contrast media with an iodine concentration of 300 mg/mL. A radiologist with six years of experience in abdominal radiology evaluated the CT scans.

We considered as the normal anatomy, the origin of the celiac trunk from the aorta, branching into the left gastric artery, the splenic artery, and the common hepatic artery. The latter, after the emergence of the gastroduodenal artery, continues as the proper hepatic artery, and branches into the RHA and left hepatic artery in the hepatic hilum (Figure 1). This was considered the typical anatomic position, and when different, it was treated as an anatomic variation, regarding its position with the pancreas, the portal vein, the common bile duct and the distance from the superior mesenteric artery and the right hepatic artery.

Figure 1
Normal anatomy of the right hepatic artery. 1A: Coronal. 1B: Axial. 1C: Sagittal. * White: Right hepatic artery.

RESULTS

A total of 5147 CT scans were analyzed. The patients’ average age was 57 ± 16.1 years, and 54.4% were men. Of those, 125 patients (2.42%) showed an anatomical variation in which RHA originated from the SMA.

Regarding the RHA position that presented variation in its origin, we observed that the most common positions were retropancreatic (88.8%) (Table 1), retroportal (76.8%) (Table 2) and posterior to the common bile duct (75, 2%) (Table 3), and the RHA emerged, on average, 2.33 (+ 0.65) cm from the SMA origin (Figure 2).

Table 1
Hepatic branch position in relation to the pancreas.
Table 2
Hepatic branch position in relation to the portal vein.
Table 3
Description of the position of the hepatic branch in relation to the common bile duct.

Figure 2
The most common anatomic position of the right hepatic artery branching from the SMA. 1A: Coronal. 1B: Axial. 1C: Sagittal. * White: Right hepatic artery.

DISCUSSION

The anatomy of the hepatic arteries has been the subject of numerous studies over the centuries. The liver, in its classical anatomy, has its arterial irrigation from the branches of the proper hepatic artery (PHA), which is a branch of the common hepatic artery (CHA)33 Sureka B, Mittal MK, Mittal A, Sinha M, Bhambri NK, Thukral BB. Variations of celiac axis, common hepatic artery and its branches in 600 patients. Indian J Radiol Imaging. 2013;23(3):223-33.,44 Venieratos D, Panagouli E, Lolis E, Tsaraklis A, Skandalakis P. A morphometric study of the celiac trunk and review of the literature. Clin Anat. 2013;26(6):741-50.. The CHA is one of the three branches that arise from the descending abdominal aorta into the celiac trunk55 Michels NA. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg. 1966;112(3):337-47.,66 Hiatt JR, Gabbay J, Busuttil RW. Surgical anatomy of the hepatic arteries in 1000 cases. Ann Surg. 1994;220(1):50-2.. The anatomy of the extrahepatic arteries is variable, which makes radiological, angiographic and surgical evaluation a difficult task77 Dilli Babu E, Poonam K. Celiac trunk variations: review with proposed new classification. Int J Anat Res. 2013;1(3):165-70..

Michels’ classic study encompassing 200 dissections, published in 1966, defined the basic anatomical variations of the hepatic arteries, and has served as a reference for the vast majority of studies in this area. This classification involves the common hepatic artery, the proper hepatic artery, and the right and left hepatic arteries. Class 1 corresponds to the normal disposition of the hepatic arterial system. Class 2 corresponds to the left hepatic artery branching from the left gastric artery. Class 3 corresponds to the RHA arising from the SMA. Class 4 refers to the multiple aberrant branches, and class 5 corresponds to the common hepatic artery branching from the SMA. Our study has assessed the class 3 position55 Michels NA. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg. 1966;112(3):337-47..

Regarding the RHA SMA-originated (Class 3), Michels described it as the most frequent variation. In the literature, there have been reports for this variation from 8% to 18%22 Fonseca-Neto OCLD, Lima HCS, Rabelo P, Melo PSV, Amorim AG, Lacerda CM. Anatomic variations of hepatic artery: a study in 479 liver transplantations. ABCD Arq Bras Cir Dig. 2017;30(1):35-7.,55 Michels NA. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg. 1966;112(3):337-47.. We believe that this variation is more relevant both for its frequency, as well as for its impact on surgical procedures in the hepatic, biliary, and pancreatic regions88 Noussios G, Dimitriou I, Chatzis I, Katsourakis A. The main anatomic variations of the hepatic artery and their importance in surgical practice: review of the literature. J Clin Med Res. 2017;9(4):248-52.,99 Yamashita K, Hashimoto D, Itoyama R, Okabe H, Chikamoto A, Beppu T, et al. Accessory right hepatic artery branched from gastroduodenal artery. Surg Case Rep. 2015;1:90.. The arterial pathway near the inferior vena cava and the portal vein is associated with the risk of inadvertent injuries while performing hepatectomies and pancreatoduodenectomies88 Noussios G, Dimitriou I, Chatzis I, Katsourakis A. The main anatomic variations of the hepatic artery and their importance in surgical practice: review of the literature. J Clin Med Res. 2017;9(4):248-52.

9 Yamashita K, Hashimoto D, Itoyama R, Okabe H, Chikamoto A, Beppu T, et al. Accessory right hepatic artery branched from gastroduodenal artery. Surg Case Rep. 2015;1:90.

10 Farghadani M, Momeni M, Hekmatnia A, Momeni F, Baradaran Mahdavi MM. Anatomical variation of celiac axis, superior mesenteric artery, and hepatic artery: evaluation with multidetector computed tomography angiography. J Res Med Sci. 2016;21:129.
-1111 Rammohan A, Palaniappan R, Pitchaimuthu A, Rajendran K, Perumal SK, Balaraman K, et al. Implications of the presence of an aberrant right hepatic artery in patients undergoing pancreaticoduodenectomy. World J Gastrointest Surg. 2014;6(1):9-13..Therefore, to identify and understand the most common course variation preoperatively is essential for those procedures.

Our study demonstrated the variants of the hepatic arterial anatomy. Detailed knowledge of these variants is essential in liver transplantation, as well as when harvesting the liver and the pancreas1212 Rebibo L, Peltier J, Gerin O, Michel D, Robert B, Regimbeau JM. Unusual course of the aberrant right hepatic artery running through the pancreatic parenchyma during modified Frey's procedure. Morphologie. 2014;98(323):182-6.. The existence of a variant of the hepatic artery can increase the risk of injury to the hepatic arterial supply leading to severe hepatic and biliary ischemia. The RHA variant originating from SMA can make it impossible to simultaneously harvest the donor’s liver and pancreas. Most complications can be prevented with the adequate identification of the vascular variants, in any of the transplant stages88 Noussios G, Dimitriou I, Chatzis I, Katsourakis A. The main anatomic variations of the hepatic artery and their importance in surgical practice: review of the literature. J Clin Med Res. 2017;9(4):248-52.,1212 Rebibo L, Peltier J, Gerin O, Michel D, Robert B, Regimbeau JM. Unusual course of the aberrant right hepatic artery running through the pancreatic parenchyma during modified Frey's procedure. Morphologie. 2014;98(323):182-6.,1313 Aragon RJ, Solomon NL. Techniques of hepatic resection. J Gastrointest Oncol. 2012;3(1):28-40..

Anatomical limitations have been extensively studied in bipartitions of liver grafts. With the different anatomical variants of the hepatic artery, the hepatic lobes can receive blood supply from the SMA, left gastric artery, aorta, or from the arterial trunk branching into other abdominal viscera. Regarding the RHA branching from the SMA trunk, this variant would favor the division between segment IV and the left lateral segment, and the division between segment IV and the right lobe. In these cases, the right lobe of the liver would be prepared along the SMA and the left lobe along the celiac trunk1414 Bertevello PL, Chaib E. [Hepatic artery system variations correlated to split-liver surgery: anatomic study in cadavers]. Arq Gastroenterol. 2002;39(2):81-5. Portuguese.,1515 Dandekar U, Dandekar K, Chavan S. Right hepatic artery: a cadaver investigation and its clinical significance. Anat Res Int. 2015; 2015:412595..

Pancreatic surgery also correlates with the arterial variants of the hepatic pedicle. The RHA branching from the SMA usually runs posteriorly along the portal vein, and between the pancreatic head and body. Although the resection of the head of the pancreas is still feasible in the presence of an arterial variant, its presence can cause significant technical difficulty, resulting in conservative resections of the pancreas. In particular, the retropancreatic dissection may result in an inadequate microscopic margin of the tumor, especially regarding the medial retroperitoneal margin. Besides, the attempt to carry out aggressive procedures, in the presence of this variant, can increase surgical time, lead to significant blood losses, and increase postoperative morbidity. However, Eshuis et al. demonstrated that when there is proper preoperative planning, the chances of successfully preserving the arterial branch variant during the intraoperative period are superior to 90%1616 Eshuis WJ, Olde Loohuis KM, Busch OR, van Gulik TM, Gouma DJ. Influence of aberrant right hepatic artery on perioperative course and longterm survival after pancreatoduodenectomy. HPB (Oxford). 2011;13(3):161-7.

17 Rubio-Manzanares-Dorado M, Marín-Gómez LM, Aparicio-Sánchez D, Suárez-Artacho G, Bellido C, Álamo JM, et al. Implication of the presence of a variant hepatic artery during the Whipple procedure. Rev Esp Enferm Dig. 2015;107(7):417-22.
-1818 Balzan SMP, Gava VG, Pedrotti S, Magalhães MA, Schwengber A, Dotto ML, et al. Prevalência de variações arteriais hepáticas com implicações em pancreatoduodenectomia. ABCD Arq Bras Cir Dig. 2019;32(3):e1455..

Reconstruction of the variant artery, using autologous grafts or synthetic materials or preoperative embolization may also be options for patients undergoing pancreatic procedures. The goal is to maintain the hepatic arterial and bile duct flow during pancreaticoduodenectomy. However, Asano et al demonstrated that the RHA resection branching from SMA can be performed in pancreatic resections even when it is technical difficult, without significantly increasing postoperative complications1919 Asano T, Nakamura T, Noji T, Okamura K, Tsuchikawa T, Nakanishi Y, et al. Outcome of concomitant resection of the replaced right hepatic artery in pancreaticoduodenectomy without reconstruction. Langenbecks Arch Surg. 2018;403(2):195-202..

We have been able to show morphometry and position variants of the RHA branching from the SMA. The frequency of these variants in the 5147 exams was 2.42%. Most studies have reported a higher frequency of the variants, over 10%. Dandekar et al. reported the variant in 22% of their sample, Eshuis et al. in 19%, Michels in 18%, and Hiatt et al. in 10,6%55 Michels NA. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg. 1966;112(3):337-47.,66 Hiatt JR, Gabbay J, Busuttil RW. Surgical anatomy of the hepatic arteries in 1000 cases. Ann Surg. 1994;220(1):50-2.,1414 Bertevello PL, Chaib E. [Hepatic artery system variations correlated to split-liver surgery: anatomic study in cadavers]. Arq Gastroenterol. 2002;39(2):81-5. Portuguese.

15 Dandekar U, Dandekar K, Chavan S. Right hepatic artery: a cadaver investigation and its clinical significance. Anat Res Int. 2015; 2015:412595.
-1616 Eshuis WJ, Olde Loohuis KM, Busch OR, van Gulik TM, Gouma DJ. Influence of aberrant right hepatic artery on perioperative course and longterm survival after pancreatoduodenectomy. HPB (Oxford). 2011;13(3):161-7..

The main strengths of our study are the number of cases and the description of the anatomic positions. We studied 125 variants of the RHA branching from the SMA, while other Brazilian authors assessed fewer patients. Fonseca-Neto et al. reported 27 cases, Balzan et al. 12 cases and Araujo et al. 3 cases11 Araujo Neto SA, Franca HA, Mello Júnior CF, Silva Neto EJ, Negromonte GRP, Duarte CMA, et al. Anatomical variations of the celiac trunk and hepatic arterial system: an analysis using multidetector computed tomography angiography. Radiol Bras. 2015;48(6):358-62.,22 Fonseca-Neto OCLD, Lima HCS, Rabelo P, Melo PSV, Amorim AG, Lacerda CM. Anatomic variations of hepatic artery: a study in 479 liver transplantations. ABCD Arq Bras Cir Dig. 2017;30(1):35-7.,1818 Balzan SMP, Gava VG, Pedrotti S, Magalhães MA, Schwengber A, Dotto ML, et al. Prevalência de variações arteriais hepáticas com implicações em pancreatoduodenectomia. ABCD Arq Bras Cir Dig. 2019;32(3):e1455.. To our knowledge our study is the first to describe the most common variants, as the retropancreatic, retroportal, posterior to the common bile duct, and branching about 2.33 cm from the SMA.

CONCLUSION

The RHA branching from the SMA is common, and its position is usually posterior to the pancreas, portal vein, and the common bile duct. Its branching is close to the emergence of the SMA from the descending abdominal aorta.

  • Source of funding: none.

REFERÊNCIAS

  • 1
    Araujo Neto SA, Franca HA, Mello Júnior CF, Silva Neto EJ, Negromonte GRP, Duarte CMA, et al. Anatomical variations of the celiac trunk and hepatic arterial system: an analysis using multidetector computed tomography angiography. Radiol Bras. 2015;48(6):358-62.
  • 2
    Fonseca-Neto OCLD, Lima HCS, Rabelo P, Melo PSV, Amorim AG, Lacerda CM. Anatomic variations of hepatic artery: a study in 479 liver transplantations. ABCD Arq Bras Cir Dig. 2017;30(1):35-7.
  • 3
    Sureka B, Mittal MK, Mittal A, Sinha M, Bhambri NK, Thukral BB. Variations of celiac axis, common hepatic artery and its branches in 600 patients. Indian J Radiol Imaging. 2013;23(3):223-33.
  • 4
    Venieratos D, Panagouli E, Lolis E, Tsaraklis A, Skandalakis P. A morphometric study of the celiac trunk and review of the literature. Clin Anat. 2013;26(6):741-50.
  • 5
    Michels NA. Newer anatomy of the liver and its variant blood supply and collateral circulation. Am J Surg. 1966;112(3):337-47.
  • 6
    Hiatt JR, Gabbay J, Busuttil RW. Surgical anatomy of the hepatic arteries in 1000 cases. Ann Surg. 1994;220(1):50-2.
  • 7
    Dilli Babu E, Poonam K. Celiac trunk variations: review with proposed new classification. Int J Anat Res. 2013;1(3):165-70.
  • 8
    Noussios G, Dimitriou I, Chatzis I, Katsourakis A. The main anatomic variations of the hepatic artery and their importance in surgical practice: review of the literature. J Clin Med Res. 2017;9(4):248-52.
  • 9
    Yamashita K, Hashimoto D, Itoyama R, Okabe H, Chikamoto A, Beppu T, et al. Accessory right hepatic artery branched from gastroduodenal artery. Surg Case Rep. 2015;1:90.
  • 10
    Farghadani M, Momeni M, Hekmatnia A, Momeni F, Baradaran Mahdavi MM. Anatomical variation of celiac axis, superior mesenteric artery, and hepatic artery: evaluation with multidetector computed tomography angiography. J Res Med Sci. 2016;21:129.
  • 11
    Rammohan A, Palaniappan R, Pitchaimuthu A, Rajendran K, Perumal SK, Balaraman K, et al. Implications of the presence of an aberrant right hepatic artery in patients undergoing pancreaticoduodenectomy. World J Gastrointest Surg. 2014;6(1):9-13.
  • 12
    Rebibo L, Peltier J, Gerin O, Michel D, Robert B, Regimbeau JM. Unusual course of the aberrant right hepatic artery running through the pancreatic parenchyma during modified Frey's procedure. Morphologie. 2014;98(323):182-6.
  • 13
    Aragon RJ, Solomon NL. Techniques of hepatic resection. J Gastrointest Oncol. 2012;3(1):28-40.
  • 14
    Bertevello PL, Chaib E. [Hepatic artery system variations correlated to split-liver surgery: anatomic study in cadavers]. Arq Gastroenterol. 2002;39(2):81-5. Portuguese.
  • 15
    Dandekar U, Dandekar K, Chavan S. Right hepatic artery: a cadaver investigation and its clinical significance. Anat Res Int. 2015; 2015:412595.
  • 16
    Eshuis WJ, Olde Loohuis KM, Busch OR, van Gulik TM, Gouma DJ. Influence of aberrant right hepatic artery on perioperative course and longterm survival after pancreatoduodenectomy. HPB (Oxford). 2011;13(3):161-7.
  • 17
    Rubio-Manzanares-Dorado M, Marín-Gómez LM, Aparicio-Sánchez D, Suárez-Artacho G, Bellido C, Álamo JM, et al. Implication of the presence of a variant hepatic artery during the Whipple procedure. Rev Esp Enferm Dig. 2015;107(7):417-22.
  • 18
    Balzan SMP, Gava VG, Pedrotti S, Magalhães MA, Schwengber A, Dotto ML, et al. Prevalência de variações arteriais hepáticas com implicações em pancreatoduodenectomia. ABCD Arq Bras Cir Dig. 2019;32(3):e1455.
  • 19
    Asano T, Nakamura T, Noji T, Okamura K, Tsuchikawa T, Nakanishi Y, et al. Outcome of concomitant resection of the replaced right hepatic artery in pancreaticoduodenectomy without reconstruction. Langenbecks Arch Surg. 2018;403(2):195-202.

Publication Dates

  • Publication in this collection
    03 June 2020
  • Date of issue
    2020

History

  • Received
    06 Oct 2019
  • Accepted
    11 Dec 2019
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