Introduction

Collateral circulation refers to the opening of the communicating branches between blood vessels when the normal vascular pathway is seriously narrowed or blocked, which alleviates the high pressure and achieves self-compensation. This plays a vital role in the blood supply and reflux of patients' liver to ensure liver function.

AE is confined to the northern hemisphere, especially restricted in such areas as central and Eastern Europe, Russia, China, northern Japan and northern region of North America [1]. It proliferates in an invasive manner, constantly produces new vesicles and penetrates into tissues, similarly as malignancy[2]. It can not only directly invade adjacent tissues, but also metastasize via lymphatic and blood supplies to retroperitoneal and distant organs, such as the brain and lungs [3, 4]. Its slow growth in the liver leads to chronic vascular occlusion, which provides sufficient time for compensatory collateral angiogenesis, with unique clinical features exhibited. When the arteries, portal vein (PV), hepatic vein (HV) and Inferior vena cava (IVC)were severely invaded, the corresponding collateral circulation may occur to maintain liver circulation and function. Not only collateral circulations arising from the particular disease but also the compensatory capacity of the hepatic vascular system was a big shock to us.

Unfortunately, except case report, there have been few reports on hepatic collateral circulation due to this particular pathogenesis. As a leading medical institution in areas with a high prevalence of echinococcosis, our center has been dedicated to its diagnosis and treatment for many years and accumulated much experience. This study explored the collateral circulation of each vascular system in liver with end-stage hepatic AE, which may help to improve our understanding of the process and complications of collateral angiogenesis caused by intrahepatic lesions and provide new ideas for surgical treatment.

Patients and methods

This retrospective case series included 51 end-stage HAE patients with collateral circulation diagnosed and treated at the digestive vascular surgery center, the First Affiliated Hospital of ** to serve as a new alternative treatment.

Fig. 3
figure 3

treatment of portal cavernous variant by ELRA: A CT image of hepatic vesicular hydatid induced portal cavernous degeneration. B Varicose vessels are seen in the hilar area. C The round ligament of the liver is catheterized to guarantee extracorporeal perfusion of the liver. D reconstruction of the portal vein with blood vessels in patients after cardiac death E anastomosis of the portal vein

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IVC

The Vascular collateralization of the IVC has been reported in details by Kapur [15], but the vertebral and lumbar veins have not been described, which may differ from the specific location of the IVC invaded by HAE. The posterior hepatic segment of IVC between the left atrium and the right renal vein was the main site involved. The collateral circulation of the IVC was thought to have two main pathways: the lumbar venous plexus and the vertebral venous plexus [16] (Fig. 4). Via the four lumbar veins symmetrical to the left and right sides and the lumbar ascending veins, left side of the lumbar venous moves into the hemiazygos vein and the right side enters the superior vena cava and returns to the atrial along the azygos vein. IVC angiography revealed that the collateral vessels of the vertebral venous plexus were dominated by the intraspinal veins, which ascended along the spinal canal. It had been reported to be an important route for communicating the superior and IVC, as well as intra—and extracranial, because of the lack of venous valves and the extensive communicating branches at other venous plexuses (intracranial venous sinus, thoracic, abdominal, pelvic venous plexus), which was of great physiological and clinical importance in the spread of infection, metastasis of tumors, and the formation of collateral circulation [17,18,19]. One patient out of 12 showed a metastatic lesion in the brain but not in the lung. Is it possible that this is the route by which neglected hepatic AE metastasize to the brain?

Fig. 4
figure 4

collateral vessels of the inferior vena cava: A vertebral venous plexus vessel shown by arrow. B Lumbar ascending vein shown by arrow C schematic representation of the collateral vessels of the inferior vena cava. D No reconstruction of the inferior vena cava. The hepatic vein is anastomosed end-to-end to the superior and inferior vena cava as indicated by the arrow

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Clinically, IVC obstruction was manifested by ascites and lower limb edema. Most patients with HAE are asymptomatic because of the well-established collateral circulation. The presence or absence of significant symptoms served as an important basis for determining whether the collateral circulation was well established after complete IVC obstruction, and played an important role in deciding which surgical approach to reconstruct the IVC. Our previous study proposed a surgical approach without reconstruction of the IVC in the presence of well-established collateral circulation, yielding good results [20, 21]. But for which careful preoperative evaluation and implementation lay the basis.

It was of concern that the collateral circulation of the inferior vena cava was difficult to observe by CT and was thus usually visualized by angiography. Therefore, once the inferior vena cava was severely obstructed, it was recommended to improve the inferior vena cava angiography to well assess whether there was collateral circulation established.

Hepatic vein

Collateral circulation of the hepatic vein has rarely been reported in other diseases. It is generally accepted that the short hepatic vein is an important compensatory vessel [22]. When the hepatic vein was obstructed, the short hepatic vein became abnormally thick and compensated for the function of the hepatic vein. In two patients, complete obstruction of the hepatic vein was followed by a dilated traffic vessel between the hepatic vein and the short hepatic vein, in which case blood flowed through the traffic branch into the short hepatic vein and then converged into the IVC (Fig. 5). Restricted by a few reports available in the form of case reports [23,24,25], we hypothesized that the appearance of intrahepatic venous plexus resulted from the original presence of fine intervening venous traffic branches in the liver, which gradually expanded and acted as mutual traffic when the main hepatic venous trunk was obstructed. However, if similar traffic vessels were lacking in the liver, the main hepatic venous reflux area would cause congestion, while the uninvolved short venous return area remained unaffected. This may have important implications for ELRA, since both the main hepatic trunk and the short hepatic veins was to be reconstructed when the liver formed thicker short hepatic veins and the remaining liver tissue remained congested. If there was an intrahepatic venous plexus and obstruction of the main hepatic trunk without obvious signs of liver congestion, it was feasible to reconstruct only the main hepatic trunk and suture the short hepatic vein. One case was reconstructed with ELRA and no significant postoperative complications occurred.

Fig. 5
figure 5

collateral vessels of the intrahepatic veins: A Angiography of the collateral vessels of the intrahepatic veins. B: Schematic representation of the collateral vessels of the intrahepatic veins

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Hepatic artery

The collateral circulation of the hepatic artery in patients with hepatic AE has rarely been reported, but it has been reported in small numbers in patients with HCC because of its particular implications for interventional treatment. We found one case in which the main hepatic artery was invaded, with an artery emanating from the coeliac trunk and running within the hepato-gastric ligament to supply blood to the healthy left liver (Fig. 6). Although it is possible that the artery could be a variant, it does also act as a blood compensation similar to collateral circulation. Phrenic artery is the most common variant of arterial blood supply for liver cancer patient, with equal origin from either the aorta or coeliac axis. It is worth exploring whether direct resection of the originally invaded arterial trunk with reconstruction of only the PV and biliary tract is feasible in patients with end-stage vesicular echinococcosis in whom arterial vascular collaterals are present and the first hepatic hilum invaded.

Fig. 6
figure 6

A–D preoperative imaging findings of the patient: A the arrow shows: the main hepatic artery is invaded B the main portal vein is invaded; C Arrow in D collateral vessel of hepatic artery. E Intraoperatively, the first hilum is seen to be severely invaded. F Red arrow: hepatic artery; Blue arrows: portal vein; Yellow arrows: intrahepatic biliary tract E reconstructed portal vein F collateral vessels of hepatic artery G: the blue arrow shows: portal vein; H: the red arrow shows: hepatic artery

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There are also many shortcomings. Due to the invasive nature of venography, not all cases in this study were observed by angiography. In addition, this study was restricted by a small sample size.

Conclusions

HAE, as a benign tumor-like disease, has its own special biological characteristics and therefore appears with collateral vessels that are difficult to present in other diseases. An in-depth study of it will be of great help to improve our understanding of the process of collateral vessel formation due to intrahepatic lesions and its comorbidity, in addition to providing new ideas for the surgical treatment of end-stage HAE.