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Keywords:

  • centrolobular hepatic fibrosis;
  • hepatic venous hypertension;
  • hepatocellular carcinoma;
  • inferior vena cavography;
  • membranous obstruction of the inferior vena cava

Abstract

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

Abstract: Although rare in most countries, membranous obstruction of the inferior vena cava (MOIVC) occurs more frequently in Nepal, South Africa, Japan, India, China, and Korea. The occlusive lesion always occurs at approximately the level of the diaphragm. It commonly takes the form of a membrane, but may be a fibrotic occlusion of variable length. Controversy exists as to whether MOIVC is a developmental abnormality or a result of organization of a thrombus in the hepatic portion of the inferior vena cava. The outstanding physical sign associated with MOIVC are large truncal collateral vessels with a cephalad flow. A dilated vena azygous is seen on chest radiography. Definitive diagnosis is made by contrast inferior vena cavography. The long-standing obstruction to hepatic venous flow causes severe centrolobular fibrosis and predisposes to the development of hepatocellular carcinoma (HCC). Percutaneous balloon angioplasty, transatrial membranotomy, or more complex vena caval and portal decompression surgery should be performed to prevent these complications. HCC occurs in more than 40% of South African Black and Japanese patients with MOIVC, but less often in other populations. It is thought to result from the tumour-promoting effect of continuous hepatocyte necrosis, although the associated environmental risk factors have not been identified.

The clinico-pathological entity described first by Lamboran (1), later by Budd (2), and then by Chiari (3), and referred to as the Budd–Chiari syndrome, comprised hepatic vein thrombosis resulting in hepatic venous outflow obstruction and centrolobular hepatic congestion. Over time, the definition of the syndrome was broadened to include other causes of hepatic venous outflow obstruction located specifically in the hepatic portion of the inferior vena cava (IVC) (4, 5). These causes are membranous obstruction of the IVC (MOIVC) and primary thrombosis of the hepatic portion of the inferior vena cava. The two conditions may be inter-related, because one theory of the origin of MOIVC is that it is the end result of thrombosis in the hepatic portion of the IVC.

MOIVC is an occlusive lesion of the IVC, usually complete but occasionally with a small central opening, which is always located close to the entry of the IVC into the right atrium or just below the level of the diaphragm. Although the obstruction is most often caused by a membrane of variable thickness across the lumen (type I) (Fig. 1), it may also take the form of a fibrotic occlusion of variable length (which may exceed 5 cm) (type II) (Fig. 2) (6, 7). In some patients, there is a stenosis of the IVC with a membrane completing the occlusion. The hepatic vein orifices may also be stenotic and that of the left hepatic vein is often, and the left, right, and middle hepatic veins are sometimes, completely occluded.

image

Figure 1.  Simultaneous inferior vena cavogram and injection of contrast medium through a catheter in the right atrium showing a thin membrane across the lumen of the inferior vena cava just below the right atrium (type I membranous obstruction of the inferior vena cava). Note that the patent right hepatic vein is dilated and shows retrograde filling with contrast medium. The left and middle hepatic veins are occluded. (Reproduced with permission.)

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image

Figure 2.  Simultaneous inferior vena cavogram and injection of contrast medium through a catheter in the right atrium showing a fibrosed occlusion 2–3 cm in length of the inferior vena cava just below the level of the diaphragm (type II membranous obstruction of the inferior vena cava). The left, right, and middle hepatic veins are occluded.

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The term obliterative hepatocavopathy has been proposed to distinguish MOIVC from hepatic vein thrombosis (8). Perhaps not surprisingly, the term has not gained wide acceptance.

Although rare in most countries (9), MOIVC occurs more frequently in Nepal (10), South Africa (7, 11), Japan (6, 12, 13), India (14, 15), China (16), and Korea (17, 18). In the countries in which MOIVC occurs more frequently, it is the most common cause of hepatic venous outflow obstruction, whereas hepatic vein thrombosis is the most common cause in all other countries.

Aetiology of membranous obstruction of the IVC

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

The cause of MOIVC is disputed. Two possible origins have been suggested – a congenital vascular malformation or the end result of organization of a thrombus localized to the hepatic portion of the IVC. Most of the early reports favoured a developmental origin (6, 7, 13). The embryological development of the upper portion of the IVC is a complex process (6, 19). Channels in the early sinusoidal labyrinth drain blood from the vitelline, umbilical, and right subcardinal veins. The proximal segment of the early right vitelline vein becomes a common drainage outlet into the sinus venosus, which later forms a part of the IVC. The ductus venosus drains blood from the left umbilical vein and channels it into the common drainage outlet. Anomalous fusions or obstructions of these sinusoidal channels may result in failure of establishment of right atrial inflow from the sinus venosus or extension of the normal obliterative process of the ductus venosus into the IVC (6, 7, 13). Indirect support for a congenital origin was provided by the failure in early studies to uncover a hypercoagulable state or other reason for thrombosis in the hepatic portion of the IVC, the lack of a compelling reason for the thrombus always to form in the same position, and difficulty in reconciling a ‘membranous’ obstruction with a thrombotic event. In addition, the histological similarity between the occluding lesion and the wall of the IVC (6) and, later, the familial occurrence of MOIVC (20), were considered to favour a developmental anomaly.

In more recent years, arguments in support of MOIVC being a consequence of organization of a thrombus in the hepatic portion of the IVC have gained momentum and the congenital origin of the lesion has been questioned. The failure to find MOIVC in foetuses, neonates, and infants and its rarity in children, the rarity of an increased frequency of associated developmental abnormalities near the MOIVC or elsewhere, and the variable anatomical pattern of the lesion are emphasized by authors favouring an acquired origin (21). Moreover, evolution over time of an IVC thrombus into membranous obstruction has been described (22), as has narrowing of the IVC progressing to complete occlusion (23). Detailed histopathological studies in Japanese patients with MOIVC have demonstrated the transition from thrombi to fibrous connective tissue and calcification, and have stressed the similarity of the end picture to that in MOIVC (24). Reports of progression of IVC thrombosis to MOIVC in patients with lupus anticoagulant (22), latent myeloproliferative disorders (25), hereditary protein C deficiency (26), primary antiphospholipid antibody syndrome (27), and hypercoagulability as a result of Factor V Leiden (28) provide further support for the thrombosis theory. In addition, recurrence of MOIVC after successful transcardiac membranotomy has been documented in two patients (29, 30). The thrombus is thought to originate usually at the ostia of the hepatic veins, and the different combinations of confluent thrombus that result may determine the variations in the final occluding lesion (21).

If transition of a thrombus to membranous or fibrous occlusion of the IVC proves to be the correct explanation for the genesis of MOIVC, the question remains: why does the initiating thrombus always occur in the hepatic portion of the IVC immediately below the entrance of the IVC into the right atrium or just below in approximate relation to the diaphragm? Three possible explanations have been offered, although there is no convincing evidence in support of any of them. Mechanical injury to the intima of the IVC in the vicinity of the diaphragm, possibly as a result of the constant movements of the diaphragm, is one suggested mechanism (31). Another is inflammation of the intima in this region on an infective basis (4, 32). This explanation has been suggested to be the cause of the frequency of MOIVC in Nepal, where this lesion accounts for more than 30% of chronic liver diseases (10). Moreover, filarial infection around the upper portion of the IVC has been reported in two patients with MOIVC (33). The third possibility is that turbulence of blood flow in the IVC at the point of hepatic venous inflow might predispose to thrombosis at this site (34). Neither the first nor the third suggested cause would explain the appreciably higher incidence of MOIVC in just a few countries.

Clinical presentation and diagnosis

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

Men comprise between 54% and 75% of patients with MOIVC (6, 7, 9, 13, 15, 25). With few exceptions (7, 35, 36), the patients have been adults, with ages ranging from the early twenties to the early seventies, but with most patients being in the twenties, thirties, and forties (6, 7, 9, 11, 13, 15, 25, 35). The symptoms of MOIVC are usually gradual in onset and have often been present for several or many years before the diagnosis is made. Intermittent or continuous pain or discomfort in the upper abdomen is the most common complaint, sometimes accompanied by intermittent or continuous swelling of the ankles. The most striking physical sign is the presence of large collateral vessels coursing over the anterior and posterior regions of the trunk (Fig. 3). The flow of blood in these collaterals is cephalad. Other less obvious clinical findings may be persistent or intermittent oedema of the lower limbs, often with venous stasis, varicose veins, pigmentation, induration, or stasis ulceration. If the deep collateral channels are well developed, dilatation of the superficial collateral vessels and oedema of the lower limbs may not be obvious. A moderately or slightly enlarged, firm liver is typically present, and the spleen may be slightly enlarged. Ascites is sometimes present. The clinical picture in MOIVC thus contrasts sharply with that of hepatic vein thrombosis, in which the symptoms are typically abrupt in onset and of short duration, with severe abdominal pain, an enlarged and tender liver, severe and intractable ascites, and obvious lower limb oedema.

image

Figure 3.  Large tortuous collateral vessels on the anterior aspect of the trunk of a South African Black patient with membranous obstruction of the inferior vena cava. The blood flow in the collateral vessels is cephalad.

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If MOIVC is suspected, a definitive diagnosis should be made because the occlusive lesion may be surgically correctable, and the complications of chronic fibrotic liver disease and hepatocellular carcinoma (HCC) may then be avoided.

The presence of a dilated vena azygos seen in the right tracheo-bronchial angle on plain postero-anterior chest radiography confirms the presence of long-standing obstruction to the IVC (37) (Fig. 4). Lobulated paravertebral opacities resulting from dilated and tortuous azygos and hemi-azygous veins may also be seen in the mid and lower dorsal regions on plain chest radiography (37). Biochemical tests show evidence of liver dysfunction, including sometimes a raised serum bilirubin concentration, but the changes are usually slight and the pattern is not helpful in the diagnosis of MOIVC. Haematological changes of hypersplenism may be found. Albuminuria may be present as a result of the IVC hypertension. Sparing of an enlarged caudate lobe (‘hot spot’) on radionuclide scanning, characteristic of hepatic vein thrombosis (38), may not be seen with MOIVC (18), and this is sometimes helpful. Ultrasonography and computed tomography with contrast enhancement may suggest the diagnosis, and oesophago-gastric varices may be seen on gastroscopy or contrast medium examination.

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Figure 4.  Postero-anterior chest radiograph showing a dilated vena azygous (arrowed) in the right tracheo-bronchial angle in a patient with membranous obstruction of the inferior vena cava.

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Radionuclide venography may be a useful screening test (39) but a definitive diagnosis requires contrast inferior vena cavography (6, 7, 9, 13, 36, 38). Because the thickness of the occlusive lesion is a crucial factor in planning the treatment of MOIVC, inferior vena cavography should be combined with visualization of the upper end of the obstruction by means of a catheter introduced into the right atrium. The left hepatic vein is commonly shown to be occluded in patients with MOIVC. The right hepatic and middle hepatic veins are usually patent and dilated (Fig. 1), although they too may be occluded. Numerous large collateral vessels are seen returning blood to the heart. Filling defects caused by thrombi may be present below and above the occlusive lesion. Transhepatic measurement of hepatic venous and portal pressures shows hepatic vein pressure to be equal to or greater than portal pressure, and intra-hepatic injection of contrast medium reveals aberrant hepatic venous drainage (38).

Liver biopsy shows the expected picture of marked centrolobular (perivenular) fibrosis (Fig. 5A and B) (7, 24). The appearance of the liver tissue does not conform to the strict definition of cirrhosis, but the liver is typically grossly scarred and may show partial expansion of nodule-like formations (40). The term reversed lobulation is sometimes used to describe the pathological appearance. The centrolobular veins and sinusoids may be mildly or moderately dilated and congested, but the severe centrolobular congestion that typifies hepatic vein thrombosis (and veno-occlusive disease) is not seen with MOIVC.

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Figure 5.  Photomicrographs of a liver section stained with haematoxylin and eosin (A) and Masson trichrome (B) from a patient with membranous obstruction of the inferior vena cava showing marked, bland centrolobular fibrosis with mild congestion. Note the normal portal tract and periportal hepatic parenchyma.

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Natural history and treatment

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

The natural history of patients with MOIVC has not been clearly defined, although the course ranges from prolonged and benign to short and fatal, with the patients surviving for periods of less than one up to 23 years (6, 7, 9, 11, 13, 15, 25, 35). Among the determinants of the natural history, the three most important are the nature of the occlusive lesion (9), the adequacy of the collateral circulation (9), and the development of HCC. Those patients in whom all three hepatic veins are occluded survive for an appreciably shorter time than those with at least one hepatic vein patent (9).

If the membrane in MOIVC has been shown to be thin, percutaneous transluminal balloon angioplasty, with or without stent placement, is usually successful (27, 41–44). With thicker membranes, transatrial membranotomy on cardiopulmonary bypass is the most commonly performed operation (6, 9, 13), although insertion of a patch graft is sometimes used. Transatrial membranotomy is not feasible for long segments of IVC occlusion. A requirement for a successful outcome of these operations appears to be patency of at least one hepatic vein (9, 13). If this requirement is not met, a two-stage operation in which transatrial membranotomy is followed by side-to-side portacaval or other form of combined portal and vena caval decompression surgery may be required (9, 44–47). A variety of less usual shunts, including meso-atrial, portal vein-right atrial, splenic vein-right atrial, and spleno-azygous shunts, have also been attempted (9). The long-term patency of these shunts is not known.

Membranous obstruction of the IVC as a cause of HCC

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

MOIVC may be complicated by the development of HCC. However, the frequency with which this complication occurs varies between geographical regions. The risk appears to be greatest in South African Blacks, in whom 40–48% of subjects with MOIVC have been found to develop HCC (7, 11) and Japanese, in whom the prevalence is 41% (48). Both of these populations have a relatively high incidence of MOIVC. The risk of HCC complicating MOIVC in other countries with a relatively high incidence of the occlusive lesion seems to be lower (11% in India and 4.7% in Nepal (49)), and appears to be lowest in countries in which MOIVC is rare, although a precise prevalence is difficult to obtain because of the small number of patients reported in these countries.

The most detailed analysis of the relationship between MOIVC and HCC was performed by Simson in South African Blacks (7). He found 48 patients with HCC in 100 Black Africans with MOIVC. Moreover, in an analysis of 44 patients with congestive hepatic fibrosis on liver biopsy, 38 (86.4%) were shown to have MOIVC on contrast inferior vena cavography. An earlier analysis from his group of necropsies suggested that as many as 20% of HCCs have an underlying MOIVC (50). However, in a later study by Kew et al. (11) of 162 unselected Black Africans with HCC seen in hospitals, not very distant from the hospitals providing Simson's patients, using radionuclide and contrast inferior vena cavography, necropsy, and laparotomy examination, MOIVC was detected in six (3.7%) patients. In this study, six of the 15 individuals (40%) found to have MOIVC had concomitant HCC. At that time, of a total of 131 Black African patients with MOIVC studied (7, 11, 51 and the updated Baragwanath Hospital series) 57 (43.5%) had HCC. The current figure (taking the two original studies together with recently updated figures from Baragwanath Hospital) is 146 patients with MOIVC, of whom 64 have HCC (45.2%).

Little information has been published on the sex distribution and ages of patients with MOIVC complicated by HCC. In the combined series of South African Black patients reported by Kew et al. (11) and those since seen at Baragwanath Hospital, the sex ratio in those with uncomplicated MOIVC was approximately equal, whereas that of patients with HCC complicating MOIVC was 2.5:1.0 in favour of males. The mean age of the South African Black patients with MOIVC and HCC reported by Kew et al. (11) was 36.7 years. These patients are significantly younger than those with MOIVC not complicated by HCC (40.7 years) (11), rural southern African Blacks with HCC from other causes (40.0 years), and urban or urbanized Blacks with HCC from other causes (50.9 years) (52).

The different risks of HCC development in patients with MOIVC in different countries or regions (11) favour the belief that malignant transformation is not a direct consequence of the occlusive lesion. Rather, the centrolobular necrosis and regeneration resulting from the hepatic venous hypertension and congestion, by acting as a tumour promoter, predisposes the individual to one or more environmental hepatocarcinogens prevalent in those countries or regions where HCC often complicates MOIVC. This belief is supported by the experience in South Africa that the risk of tumour formation in these patients is significantly greater (at the 1% level) in the old Transvaal province (now Gauteng, Northern, North-west, and Mpumulanga provinces) than in other provinces of South Africa or in neighbouring countries (11). Because the risk of malignant transformation is greatest in South African Blacks and Japanese, environmental aetiological factors that should be considered in this respect would be hepatitis B virus (HBV) and aflatoxin B1 in the former, and hepatitis C virus (HCV) and, to a lesser extent, HBV, in the latter. Simson reported a prevalence of HBV of 22% in his patients with MOIVC and HCC (7), but this is far less than the prevalence of this virus in all Black Africans with HCC of comparable age to those with MOIVC (53, 54). Furthermore, hepatitis B surface antigen was not detected in the serum of any of the patients with HCC complicating MOIVC in the study of Kew et al. (11) or in a number of reports in the literature of one or a small number of patients in whom the antigen was tested for. Nor is the prevalence of HBV-induced HCC higher in the old Transvaal province than it is in other provinces or other southern African countries. No obvious correlation with dietary exposure to aflatoxin B1, alcohol abuse, or cigarette smoking was found in the published report (11) or has been found since (unpublished data). No study of the possible role for HCV in HCC complicating MOIVC in Japanese patients has been reported, although such an association has not been shown in Black Africans (unpublished data) or in the few reports of occasional patients with MOIVC from other populations in whom the presence of the HCV has been tested for. An environmental hepatocarcinogen responsible for HCC complicating MOIVC has, thus, not yet been identified. The South African experience raises the possibility that either a deficiency or an excess of some chemical in the soil and hence in the diet might be implicated.

Acknowledgements

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References

The authors are grateful to Professor A. C. Paterson for Fig. 5 A and B. Figure 1 was reprinted from Kimura C, Matsuda S, Koie H, et al: Membraneous obstruction of the hepatic portion of the inferior vena cava: clinical study of 9 cases. Surgery 1972: 72, 551–559, with permission from Elsevier.

References

  1. Top of page
  2. Abstract
  3. Aetiology of membranous obstruction of the IVC
  4. Clinical presentation and diagnosis
  5. Natural history and treatment
  6. Membranous obstruction of the IVC as a cause of HCC
  7. Acknowledgements
  8. References
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