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Effectiveness and Postoperative Prognosis of Using Preopening and Staged Percutaneous Transluminal Angioplasty of the Inferior Vena Cava in Treating Budd-Chiari Syndrome Accompanied with Inferior Vena Cava Thrombosis
Clinical Research Effectiveness and Postoperative Prognosis of Using Preopening and Staged Percutaneous Transluminal Angioplasty of the Inferior Vena Cava in Treating Budd-Chiari Syndrome Accompanied with Inferior Vena Cava Thrombosis Chaowen Yu, Yong Gao, Zhonglin Nie, Tao Song, Shiyuan Chen, Ran Lu, and Wenbo Tang, Bengbu, People’s Republic of China
Background: Budd-Chiari syndrome (BCS) is a rare disorder that has relatively high prevalence in the Huang-Huai area of China. Effective treatment of BCS accompanied with inferior vena cava thrombosis is challenging. Objective: This study retrospectively analyzed the clinical effectiveness and safety of traditional open operations versus preopening and staged percutaneous transluminal angioplasty (PTA) of the inferior vena cava in treating BCS accompanied with inferior vena cava thrombosis. Methods: Data from patients hospitalized and treated for BCS accompanied with inferior vena cava thrombosis between January 1997 and December 2017 were retrospectively analyzed. Thirty-two patients received traditional open operation (open group). Fifty-six patients received preopening and staged PTA of the inferior vena cava (PTA group). Baseline and clinical data were compared between groups. The patients were followed for up to 60 months. Postoperative recurrence rates and restenosis degree were recorded. Results: Eighty-eight patients were included (47 males and 41 females), aged 41.82 ± 10.12 years (range 29e65). In the open group, no pulmonary arterial embolism was found during and after the operation, and the technique success rate was 100%. One patient died of intrathoracic bleeding. In the PTA group, 2 patients had shifting of thrombus in the inferior vena cava that blocked the blood flow restored by the preopening, one resulted in treatment failure, while the other had blood flow restored by dilation with a 12-mm balloon; the success rate was 55/56 (98.21%). The median follow-up time was 32 months (range 3e60). Two patients in the open group developed restenosis 2 years after operation (recurrence rate: 6.25%), and were successfully treated by balloon PTA. Seven patients in the PTA group had severe restenosis 18e42 months after operation (recurrence rate: 12.96%). No thrombosis was found in these 7 patients, and normal blood flow was restored in the inferior vena cava after balloon PTA. Conclusions: Preopening and staged PTA of the inferior vena cava is a safe and simple method for the treatment of BCS accompanied with inferior vena cava thrombosis, with satisfactory treatment effectiveness that could be applied in clinical practice.
Chaowen Yu and Yong Gao contributed equally to this work. Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest: The authors declare that they have no conflict of interest. Department of Vascular Surgery, The First Affiliated Hospital of Bengbu Medical College, Bengbu, People’s Republic of China.
Correspondence to: Yong Gao, Department of Vascular Surgery, The First Affiliated Hospital of Bengbu Medical College, Bengbu, People’s Republic of China; E-mail: [email protected] Ann Vasc Surg 2019; -: 1–9 https://doi.org/10.1016/j.avsg.2019.03.037 Ó 2019 Elsevier Inc. All rights reserved. Manuscript received: January 2, 2019; manuscript accepted: March 8, 2019; published online: - - -
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INTRODUCTION Budd-Chiari syndrome (BCS) is a relatively rare disease worldwide that can be fatal if not correctly treated.1 BCS is defined as hepatic venous outflow obstruction at any level from the small hepatic veins to the junction of the inferior vena cava and the right atrium resulting from thrombosis or its fibrous sequelae.2 Therefore, BCS is a complex disease that presents with a variety of etiologies.3 BCS is highly prevalent in the Huang-Huai area of China, but the etiologies are still unclear. The common clinical pathological types of BCS include membranous obstruction of inferior vena cava and partial segment blockage of inferior vena cava.4 Over 6,000 cases of BCS have already been treated, and guidance for the diagnosis and treatment of BCS is already available, which involves relatively simple methods for clinical diagnosis and treatment, with good outcomes.5e7 These include anticoagulation therapy, percutaneous angioplasty, transjugular intrahepatic portosystemic shunt, and liver transplantation.8e11 In China, the preferred treatment method is interventional therapy,5 but for one of the complex types of BCS, namely BCS accompanied with inferior vena cava thrombosis, traditional interventional therapy could easily induce acute pulmonary artery embolism, so this has been regarded as a contraindication for its use.12e14 Inferior vena cava thrombosis is involved in around 20% of BCS cases.15 Therefore, effective treatment methods are needed. Although researchers have also used stenting to reduce embolism, catheterization for thrombolysis, and mechanical ablation treatment, which have certain degree of treatment effectiveness, such treatments do not completely clear thrombi from the inferior vena cava.11,16e19 Therefore, pulmonary artery embolism is still inevitable after percutaneous transluminal angioplasty (PTA) of the inferior vena cava. Thus, although these methods involve low mortality rate, they are not widely applied in clinical practice. In practice, conventional open radical surgery is mainly used for the early treatment of BCS with inferior vena cava thrombosis.14 During the procedure, lesions of the inferior vena cava are resected and the thrombus is completely removed under direct vision. Although such treatment has definite therapeutic effects and good prognosis, several disadvantages such as complex operation procedures, substantial intraoperative blood loss, high risk of the operation, and various postoperative complications have restricted this method to being conducted in large hospitals with a high level of experience of the procedure.
Annals of Vascular Surgery
In our medical center, preopening and staged PTA of the inferior vena cava has been used for the treatment of BCS accompanied with inferior vena cava thrombosis. This procedure has become the major treatment method for BCS with inferior vena cava thrombosis instead of open surgery. Therefore, to investigate the effectiveness and safety of this method, here we compared the 2 methods (open procedure and PTA) that had been used in our clinic to help others select the ideal treatment method.
MATERIALS AND METHODS Patients This is a retrospective analysis of data from patients with BCS with inferior vena cava thrombosis treated at the Department of Vascular Surgery of the First Affiliated Hospital of Bengbu Medical College between January 1997 and December 2017. The inclusion criteria were: (1) patients with confirmed diagnosis of BCS accompanied with inferior vena cava thrombosis by clinical manifestations and imaging examinations on admission (Fig. 1A, E, F); (2) patients’ liver functions were slightly abnormal, and the examinations of the cardiac and pulmonary functions suggested that they could tolerate the operation; and (3) the patients received either an open surgical procedure or preopening and PTA. This study has been approved by the Ethics Committee of our hospital. Study Design For the patients in the open group (n ¼ 32), conventional open surgery, namely resection of the lesions in inferior vena cava, removing thrombus, and consequent revascularization were conducted under direct vision. For the patients in the PTA group (n ¼ 56), preopening and staged PTA of the inferior vena cava were conducted. The patients in the open group received the open procedure during the earlier time period (from January 1997 to December 2010) and had both new or old thrombi in the inferior vena cava, while the patients in the PTA group who received interventional therapy later (from January 2010 to December 2017) mainly had a new thrombus in the inferior vena cava, with lesions in the partial segment of the inferior vena cava. There was 1 year (2010) during which the open procedures were gradually replaced by preopening and staged PTA of the inferior vena cava.
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Fig. 1. Open radical treatment. (A) Inferior vena cava venography shows BCS accompanied with inferior vena cava thrombosis; (B) thrombus can be seen after resecting the inferior vena cava; (C) the lesion and thrombus in the inferior vena cava; (D) suturing the wound of the inferior vena cava; (E, F) varicosity on the thoracic and abdominal walls, as well as swollen belly of the patient before operation; and (G, H) varicosity on the thoracic and abdominal walls, as well as swollen belly of the patient disappeared after the operation. For the interventional therapy, namely preopening and staged PTA of the inferior vena cava in this study (Fig. 2), the patients were treated in the interventional treatment room under local anesthesia. Catheterization via the femoral vein or bidirectional catheterization via the femoral and jugular veins was conducted. First, DSA of the inferior vena cava was conducted after catheterization to further confirm the lesions and thrombus in the inferior vena cava. For the cases with partial segment blockage, bidirectional venography was needed to clarify the length and angle of the lesion in the inferior vena cava, and a super-hard guidewire was used for the puncture via the cervical and/or femoral vein. A small balloon with a diameter of about 6e10 mm was selected according to the size and time of formation of the thrombus to dilate the involved segment for PTA and preopening (Fig. 2A). The process only involved a single dilation of the blood vessel, which avoided the damage of multiple
dilations on the thrombus in the inferior vena cava, and therefore reduced the risk of drop-off. Venography showed that blood could flow through the inferior vena cava, while the thrombus was evidently not moved. A pigtail catheter was inserted for thrombolysis (600,000e 800,000 units of urokinase, injected into the catheter in 2e3 times) for 3e5 days (Fig. 3A). During the postoperative hospital stay (5e7 days), subcutaneous injection of low molecular weight heparin (5,000 units, every 12 hr) for anticoagulation was performed, which was changed to oral intake of warfarin before discharge (the dose was adjusted according to the prothrombin time and international nomalized ratio monitoring results). The patients were hospitalized again 1 month later, and interventional therapy was conducted after sufficient preparation. During the operation, an appropriate caliber balloon was selected according to the situation of thrombolysis in the inferior vena cava, as shown in venography, to dilate the involved segment (Fig. 2B). Staged interventional therapy was conducted every 1e3 months; until the thrombus in the inferior vena cava had completely disappeared, a 20- to 25-mm diameter balloon was used to dilate the lesion area until satisfactory effects were obtained (Figs. 2C and 3B) (namely, stenosis of the inferior vena cava was 30%), and then oral intake of warfarin was continued for 6 months to 2 years after successful therapy.
Treatment Methods
vena cava was conducted, and a balloon Foley catheter was used to block the distal end of the inferior vena cava. The lesion in the inferior vena cava was resected and the thrombus in the inferior vena cava was completely removed under direct vision (Fig. 1B, C). According to the disease conditions at the inferior vena cava, direct suturing (diaphragm), patching expansion revascularization (Fig. 1D) (diaphragm or partial segment blockage), or orthotopic
Open operation was conducted under inhalation general anesthesia. An incision was made on the left chest, the pericardium and part of the diaphragm were resected, and the retrohepatic segment of the inferior vena cava (RHSIVC) and the right atrial portal vein were fully dissected. Cuff-blocking of the proximal end of the inferior
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Fig. 2. Treatment of a case in the PTA group. (A) An 8mm balloon was used for predilation (a, venography of the inferior vena cava shows BCS accompanied with inferior vena cava thrombosis; b, an 8-mm balloon was used to dilate the lesion area; c, venography after operation showed that blood flowed through the lesion area, while the shape of thrombus had not changed). (B) A 10-mm balloon was used for dilation (a, venography of the inferior vena cava showed that most of the thrombus had disappeared; b, the 10-mm balloon was used to dilate
the lesion again; c, venography showed that blood flowed satisfactorily in the inferior vena cava, and the shape of the thrombus is not changed). (C) An 18-mm balloon was used for dilation (a, venography of the inferior vena cava showed that the thrombus had disappeared; b, an 18-mm balloon was used for dilation again; and c, postoperative venography showed that blood flow in the inferior vena cava was generally smooth).
artificial blood vessel transplantation (partial segment blockage) was conducted. An autologous blood transfusion device was used to retransfuse the surgical bleeding during surgery. The varicose vessels at the surgical incision were treated by ligation and electrocoagulation for hemostasis.
compliance of the patients. Then the follow-up was changed to every 6 months during the second year after operation, and the last follow-up was generally 60 months after operation, which varied according to the compliance of the patients. Color Doppler ultrasonography was generally used for follow-up examinations, but computed tomographic venography (CTV) was used for some patients. In addition, other indexes were also collected during follow-up: liver function, high pressure of the inferior vena cava, ascites, thrombus
Follow-up In the first year after operation, the patients were followed every 1e3 months, according to the
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Fig. 3. Treatment of a second case in the PTA group. (A) An 8-mm balloon was used for predilation (a, venography of the inferior vena cava showed BCS accompanied with inferior vena cava thrombosis; b, an 8-mm balloon was used to dilate the lesion; and c, pigtail catheter was inserted for thrombolysis, venography showed that blood flowed through the inferior vena cava, and
the shape of the thrombus changed slightly). (B) A 20mm balloon was used for dilation (a, venography showed that the thrombus in the inferior vena cava had completely disappeared; b, a 20-mm balloon was used for dilation again; and c, venography after operation showed that blood flowed smoothly in the inferior vena cava).
in the inferior vena cava, and stenosis rate of the lesion area in the inferior vena cava.
patients, 59 had membranous obstruction of the inferior vena cava accompanied with thrombus, and 29 had short segment blockage of the inferior vena cava accompanied with thrombus. The clinical manifestations of the patients mainly included abdominal distension, varicosity on the thoracic and abdominal walls, splenomegaly, ascites (62 patients), edema of both lower extremities, and superficial varicosis. Some patients also presented with hyperpigmentation or ulcers. Seventeen patients had a history of upper gastrointestinal hemorrhage before hospitalization, which mainly manifested as hematemesis or melena. In addition, 59.09% (52/ 88) of the patients had been treated in other hospitals for liver cirrhosis or ascites. Color Doppler ultrasonography of blood vessels showed membranous obstruction of the RHSIVC or partial segment blockage of inferior vena cava, while the distal lumen of the blood vessel showed solid echo, with part of limited movement. CTV of the inferior vena cava of 50 patients showed
Statistical Analysis SPSS 19.0 (IBM Corp., USA) was used for statistical analysis. Quantitative data were described with means and standard divisions, and t-test was used for the comparison. Qualitative data were compared with chi-squared test. P < 0.05 was considered statistically significant.
RESULTS Baseline Characteristics Totally, 88 patients (including 47 males and 41 females) were included in this study (Table I). The mean age of the patients was 41.82 ± 10.12 years (range 29e65), and the mean disease duration was 10.28 ± 5.66 months (range 2e24). Among these
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Table I. General characteristics of the patients included in the study
n Male/female Age (years) Membranous obstruction type, n Partial segment blockage type, n Disease duration (months) Ascites, n Hepatomegaly, n Splenomegaly, n Upper gastrointestinal hemorrhage, n Edema of both lower extremities, n Varicosity of both lower extremities, n
Open group
PTA group
P-value
32 17/15 40.68 ± 10.95 20 12 10.85 ± 5.27 22 8 30 6 32 26
56 30/26 41.85 ± 10.06 39 17 11.02 ± 6.15 40 17 53 11 56 42
0.9678 0.6126 0.4929 0.4929 0.8959 0.7911 0.5919 0.7607 0.9187 1.0000 0.5009
membranous obstruction of the RHSIVC or partial segment blockage of inferior vena cava (length 25e50 mm, mean length 40.12 mm), and the distal part of the inferior vena cava had filling defects of different sizes and shapes. Normal images of the hepatic vein were found in 43 patients, while the others showed evidence of an accessory hepatic vein. Routine catheterization of the inferior vena cava was conducted before interventional therapy for digital subtraction angiography (DSA) and venography of the inferior vena cava, which showed dilation of the segment distal to the blockade in 38 patients, with large filling defects and no evident movement. Attachment and contrast agent retention were found in most patients. The findings in venography of the hepatic vein were similar to the findings in CTV. Perioperative Characteristics The procedures in the open group were all successful, with a mean operation time of 7.56 ± 0.25 hr, and mean intraoperative blood loss volume of 6,500.89 ± 150.20 mL (Table II). All the blood was transfused back to the patient via extracorporeal circulation. No pulmonary embolism was found during and after the operation, and the technical success rate was 100%. One patient in this group died of intrathoracic bleeding after the operation. In the PTA group, 2 patients experienced thrombus shifting that blocked the preopened blood flow by venography during the second treatment. One of these patients could not receive interventional therapy due to enlargement of the thrombus in the inferior vena cava and was considered to have treatment failure, and the other patient had restored blood flow after dilation with a 12-mm balloon. The treatments in all the other patients were successful, and the treatment success rate was 98.21% (55/56). The
total treatment times in this group were 3e6 times for each patient, with a mean treatment times of 4.15. None of the patients received stenting after PTA. The mean treatment time of a single intervention was 2.15 ± 0.25 hr, and the mean blood loss volume was 50.65 ± 5.92 mL. Inferior vena cava hypertension alleviated after the operation, ascites disappeared gradually, and liver function (indicated by total bilirubin, serum prealbumin, and albumin levels) improved. The mean hospital stay was 14.18 ± 1.36 and 5.87 ± 1.02 days for the patients in the open group and PTA group, respectively. Follow-up All patients were followed regularly, with mean follow-up time of 32 months (range 3e60). Color Doppler ultrasonography of the inferior vena cava was used to assess the degree of restenosis, which showed that 2 patients in the open group had stenosis of the inferior vena cava evident 2 years after operation, which was then treated with balloon dilation and angioplasty. Thus, the recurrence rate in the open group was 6.25% (2/32). In the PTA group, 7 patients had severe restenosis (stenosis rate >50%) at 18e42 months after operation, and the recurrence rate was 12.96% (7/54). No new thrombosis was found in the PTA group. Interventional therapy was further conducted for balloon dilation in these 7 patients, which successfully restored the normal blood flow in the inferior vena cava.
DISCUSSION In this study, we retrospectively analyzed the data of 2 groups of patients with BCS with thrombus in
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Table II. Comparison of perioperative data between the 2 groups
n Operation time (hr)a Intraoperative blood loss (mL) Operative death, n Technical success rate (%) Single hospital stay (days)a Postoperative recurrence rate (%) a
Open group
PTA group
P-value
32 7.56 ± 0.25 6,500.89 ± 150.20 1 100 14.18 ± 1.36 6.25
56 2.15 ± 0.25 50.65 ± 5.92 0 98.21 5.87 ± 1.02 12.96
<0.00010 <0.0001 0.7756 0.7756 <0.0001 0.5720
For each interventional session (i.e., 1 session in the open group and 3e6 sessions in the PTA group).
the inferior vena cava that was treated at our center by open or PTA methods to investigate the effectiveness and safety of these treatments. The results showed that the conventional radical open operation had several disadvantages, including complex operation procedures, long operation time, large volume of intraoperative blood loss, and various postoperative complications. In contrast, preopening of the inferior vena cava and staged PTA had evident clinical advantages, which were more pronounced regarding safety, minimal invasion, and rapid recovery. In addition, the PTA method could be used on a wider range of patients including those with indications that suggested they could not tolerate an open operation. The effectiveness of the PTA method used in this study was as high as 98.2% in the 56 patients included in the PTA group, which compares well with other studies. Meng et al.20 found that they achieved effective treatment in 96.4% of 55 similar patients using balloon dilation with stent placement and thrombus aspiration. Another study used recoverable stents with agitation thrombolysis or catheter-directed thrombolysis of the inferior vena cava in 40 patients and achieved 100% success; however, the stents were removed successfully in only 92.1% of patients and there was a case of acute pulmonary embolism.21 While a small study on 17 patients suggested 100% effectiveness with combined thrombus aspiration and inferior vena cava recanalization.22 Therefore, these studies support our data that suggest that interventional therapy is a suitable approach for treating patients with BCS with inferior vena cava thrombosis and methods not involving stents may be preferable. Preopening of the inferior vena cava to provide a small lumen restored the blood flow in the inferior vena cava to a degree, which could change the vortex of blood flow to forward blood flow. The anticoagulation and direct thrombolysis that accompanied the procedure also induced lysis of the thrombus. The overall structure of the thrombus was not
damaged during the treatment, and the blood flow in a 6- to 10-mm wide inferior vena cava not only insured the patency and forward direction of blood flow, but also avoided thrombus shifting from too strong a blood flow to block the newly formed lumen (this occurred in only 2 patients in this study, resulting in treatment failure in one of them). The risk of the thrombus falling off into the right atrium to induce pulmonary embolism was also avoided. In staged PTA, balloons with different diameters were selected according to the thrombolysis situation in the inferior vena cava, and therefore gradually opened the vein to restore normal blood flow. The authors speculate that a newly formed thrombus could be rapidly lysed, but the relatively high risk of shifting should also be considered. Therefore, we suggest caution when choosing the balloons, those with large diameters should not be selected. In contrast, an old thrombus has generally adhered to the blood vessel wall and is unlikely to fall off, although the lysis of the thrombus is relatively slow. Nevertheless, choosing balloons for such cases is more flexible, and we think that the diameter of the balloon should be about half of the diameter of the thrombus. Ensuring the safety of interventional therapy during the first predilation of the inferior vena cava provided a basis for the successful staged dilation. Staged PTA was very safe and easy to perform. Although the overall treatment duration was relatively long, every single hospital stay was very short. In addition, the success rate of the treatment was very high, and the clinical effectiveness was definite. In this study, 55 of the 56 patients were successfully treated, and the success rate was as high as 98.21%. There are several issues we should consider during interventional therapy. First, the first preopening of inferior vena cava is the key process in treating BCS accompanied with inferior vena cava thrombosis. Such preopening is relatively easy for the patients with membranous obstruction, but harder for those with partial segment blockage,
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because of different anatomic angles (lefteright or anterioreposterior angles). Therefore, opening in the patients with partial segment blockage of inferior vena cava could easily create a false lumen, and dilation could lead to serious outcomes such as pericardial tamponade or major hemorrhage. We suggest that the following should be considered: (1) sufficiently review of the CTV images before operation to clarify the anatomic angles of the inferior vena cava, which could provide evidence for the selection of appropriate angle for puncture in interventional therapy; (2) according to the preoperative assessment, the ‘‘C’’ shaped branch of DSA should be rotated appropriately; and (3) bidirectional puncture should be conducted, with a pigtail catheter inserted in the contrary end, and the proximal end should be used for guidance, which could increase the puncture success rate and the accuracy of the chosen direction. In order to ensure the safety and effectiveness of staged dilation, the following should also be considered: (1) a 1-month interval between 2 dilations is best for the patients, as a shorter interval prevents thrombolysis, and a longer interval could lead to reobstruction of the opened blood vessel; (2) the shape and structure of the thrombus should not be damaged to avoid partial fall of the thrombus; and (3) the interval between the staged dilation could be selected according to the results of the color Doppler ultrasonography of the inferior vena cava. Each dilation must not be conducted too quickly; we only dilate the lesion to a normal anatomic caliber after the thrombus in the inferior vena cava has completely disappeared; and (4) the treatment duration should be sufficient, and the postoperative anticoagulation must be adequate, which assists thrombosis and prevents postoperative recurrence of thrombosis. There are several limitations in this study. First, this is a retrospective study and the data of the 2 groups were from different time periods because the interventional therapy needed to be developed before we could use it for vascular disorders. This time difference is likely to have introduced some bias into patient grouping. In addition, the overlap of the 2 methods in 2010 could have introduced additional bias. Second, as the data were retrospective, the data were not always complete and homogeneous between groups. Although the investigators tried different methods in analyzing the data, we still could not ensure standardization of the treatment methods, or the homogeneity of the observational endpoints, which could lead to bias in the assessment of treatment effectiveness and safety profiles.
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CONCLUSIONS Preopening and staged PTA of inferior vena cava is a safe and simple method for the treatment of BCS accompanied with inferior vena cava thrombus, which had satisfactory clinical effectiveness and is applicable in clinical practice. REFERENCES 1. Hefaiedh R, Cheikh M, Marsaoui L, et al. The Budd-Chiari syndrome. Tunis Med 2013;91:376e81. 2. Valla DC. Primary Budd-Chiari syndrome. J Hepatol 2009;50:195e203. 3. Ferral H, Behrens G, Lopera J. Budd-Chiari syndrome. AJR Am J Roentgenol 2012;199:737e45. 4. Dang XW, Xu PQ, Ma XX, et al. Surgical treatment of BuddChiari syndrome: analysis of 221 cases. Hepatobiliary Pancreat Dis Int 2011;10:435e8. 5. Qi XS, Ren WR, Fan DM, et al. Selection of treatment modalities for Budd-Chiari Syndrome in China: a preliminary survey of published literature. World J Gastroenterol 2014;20:10628e36. 6. Seijo S, Plessier A, Hoekstra J, et al. Good long-term outcome of Budd-Chiari syndrome with a step-wise management. Hepatology 2013;57:1962e8. 7. Clark PJ, Slaughter RE, Radford DJ. Systemic thrombolysis for acute, severe Budd-Chiari syndrome. J Thromb Thrombolysis 2012;34:410e5. 8. Zhang F, Wang C, Li Y. The outcomes of interventional treatment for Budd-Chiari syndrome: systematic review and meta-analysis. Abdom Imaging 2015;40:601e8. 9. Meng QY, Sun NF, Wang JX, et al. Endovascular treatment of Budd-Chiari syndrome. Chin Med J (Engl) 2011;124: 3289e92. 10. Lei AW, Ruizhao Q, Zhendong Y, et al. Method and safety analysis of interventional treatment of Budd-Chiari syndrome in 1246 patients. Chin J Digestive Surg 2016;15:702e8. 11. Shen Q, Xue HZ, Jiang QF, et al. Surgical treatment of BuddChiari syndrome with hepatic inferior vena cava occlusion and thrombosis by interposition graft caval-atrial shunt. Chin J Hepatobiliary Surg 2011;17:334e6. 12. Ding PX, Li YD, Han XW, et al. Treatment of Budd-Chiari syndrome with urokinase following predilation in patients with old inferior vena cava thrombosis. Radiol Med 2011;116:56e60. 13. Zhang QQ, Xu H, Zu MH, et al. Strategy and long-term outcomes of endovascular treatment for Budd-Chiari syndrome complicated by inferior vena caval thrombosis. Eur J Vasc Endovasc Surg 2014;47:550e7. 14. Li XQ, Wu YM, Zhou WM, et al. The diagnosis and treatment of Budd-Chiari syndrome with inferior vena cava thrombosis. Chin J Gen Surg 2002;17:27e8. 15. Han XW, Ding PX, Li YD, et al. Retrieval stent filter: treatment of Budd Chiari syndrome complicated with inferior vena cava thrombosisdinitial clinical experience. Ann Thorac Surg 2007;83:655e60. 16. Ren JZ, Huang GH, Ding PX, et al. Outcomes of thrombolysis with and without predilation of the inferior vena cava (IVC) in patients with Budd-Chiari syndrome with old IVC thrombosis. Vasc Endovascular Surg 2013;47:232e8. 17. Liu L, Qi XS, Zhao Y, et al. Budd-Chiari syndrome: current perspectives and controversies. Eur Rev Med Pharmacol Sci 2016;20:3273e81.
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18. Wang YL, Ding PX, Li YD, et al. Comparative study of predilation with stent filter for Budd-Chiari syndrome with old IVC thrombosis: a nonrandomized prospective trial. Eur J Radiol 2012;81:1158e64. 19. Gao Y, Chen S, Yu C. Applicability of different endovascular methods for treatment of refractory Budd-Chiari syndrome. Cell Biochem Biophys 2011;61:453e60. 20. Meng X, Lv Y, Zhang B, et al. Endovascular management of Budd-Chiari syndrome with inferior vena cava thrombosis:
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a 14-year single-center retrospective report of 55 patients. J Vasc Interv Radiol 2016;27:1592e603. 21. Bi Y, Chen H, Ding P, et al. Long-term outcome of recoverable stents for Budd-Chiari syndrome complicated with inferior vena cava thrombosis. Sci Rep 2018;8:7393. 22. Fu YF, Xu H, Wu Q, et al. Combined thrombus aspiration and recanalization in treating Budd-Chiari syndrome with inferior vena cava thrombosis. Radiol Med 2015;120: 1094e9.
Background: Budd-Chiari syndrome (BCS) is a rare disorder that has relatively high prevalence in the Huang-Huai area of China. Effective treatment of BCS accompanied with inferior vena cava thrombosis is challenging. Objective: This study retrospectively analyzed the clinical effectiveness and safety of traditional open operations versus preopening and staged percutaneous transluminal angioplasty (PTA) of the inferior vena cava in treating BCS accompanied with inferior vena cava thrombosis. Methods: Data from patients hospitalized and treated for BCS accompanied with inferior vena cava thrombosis between January 1997 and December 2017 were retrospectively analyzed. Thirty-two patients received traditional open operation (open group). Fifty-six patients received preopening and staged PTA of the inferior vena cava (PTA group). Baseline and clinical data were compared between groups. The patients were followed for up to 60 months. Postoperative recurrence rates and restenosis degree were recorded. Results: Eighty-eight patients were included (47 males and 41 females), aged 41.82 ± 10.12 years (range 29e65). In the open group, no pulmonary arterial embolism was found during and after the operation, and the technique success rate was 100%. One patient died of intrathoracic bleeding. In the PTA group, 2 patients had shifting of thrombus in the inferior vena cava that blocked the blood flow restored by the preopening, one resulted in treatment failure, while the other had blood flow restored by dilation with a 12-mm balloon; the success rate was 55/56 (98.21%). The median follow-up time was 32 months (range 3e60). Two patients in the open group developed restenosis 2 years after operation (recurrence rate: 6.25%), and were successfully treated by balloon PTA. Seven patients in the PTA group had severe restenosis 18e42 months after operation (recurrence rate: 12.96%). No thrombosis was found in these 7 patients, and normal blood flow was restored in the inferior vena cava after balloon PTA. Conclusions: Preopening and staged PTA of the inferior vena cava is a safe and simple method for the treatment of BCS accompanied with inferior vena cava thrombosis, with satisfactory treatment effectiveness that could be applied in clinical practice.
Chaowen Yu and Yong Gao contributed equally to this work. Funding: This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors. Conflict of interest: The authors declare that they have no conflict of interest. Department of Vascular Surgery, The First Affiliated Hospital of Bengbu Medical College, Bengbu, People’s Republic of China.
Correspondence to: Yong Gao, Department of Vascular Surgery, The First Affiliated Hospital of Bengbu Medical College, Bengbu, People’s Republic of China; E-mail: [email protected] Ann Vasc Surg 2019; -: 1–9 https://doi.org/10.1016/j.avsg.2019.03.037 Ó 2019 Elsevier Inc. All rights reserved. Manuscript received: January 2, 2019; manuscript accepted: March 8, 2019; published online: - - -
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INTRODUCTION Budd-Chiari syndrome (BCS) is a relatively rare disease worldwide that can be fatal if not correctly treated.1 BCS is defined as hepatic venous outflow obstruction at any level from the small hepatic veins to the junction of the inferior vena cava and the right atrium resulting from thrombosis or its fibrous sequelae.2 Therefore, BCS is a complex disease that presents with a variety of etiologies.3 BCS is highly prevalent in the Huang-Huai area of China, but the etiologies are still unclear. The common clinical pathological types of BCS include membranous obstruction of inferior vena cava and partial segment blockage of inferior vena cava.4 Over 6,000 cases of BCS have already been treated, and guidance for the diagnosis and treatment of BCS is already available, which involves relatively simple methods for clinical diagnosis and treatment, with good outcomes.5e7 These include anticoagulation therapy, percutaneous angioplasty, transjugular intrahepatic portosystemic shunt, and liver transplantation.8e11 In China, the preferred treatment method is interventional therapy,5 but for one of the complex types of BCS, namely BCS accompanied with inferior vena cava thrombosis, traditional interventional therapy could easily induce acute pulmonary artery embolism, so this has been regarded as a contraindication for its use.12e14 Inferior vena cava thrombosis is involved in around 20% of BCS cases.15 Therefore, effective treatment methods are needed. Although researchers have also used stenting to reduce embolism, catheterization for thrombolysis, and mechanical ablation treatment, which have certain degree of treatment effectiveness, such treatments do not completely clear thrombi from the inferior vena cava.11,16e19 Therefore, pulmonary artery embolism is still inevitable after percutaneous transluminal angioplasty (PTA) of the inferior vena cava. Thus, although these methods involve low mortality rate, they are not widely applied in clinical practice. In practice, conventional open radical surgery is mainly used for the early treatment of BCS with inferior vena cava thrombosis.14 During the procedure, lesions of the inferior vena cava are resected and the thrombus is completely removed under direct vision. Although such treatment has definite therapeutic effects and good prognosis, several disadvantages such as complex operation procedures, substantial intraoperative blood loss, high risk of the operation, and various postoperative complications have restricted this method to being conducted in large hospitals with a high level of experience of the procedure.
Annals of Vascular Surgery
In our medical center, preopening and staged PTA of the inferior vena cava has been used for the treatment of BCS accompanied with inferior vena cava thrombosis. This procedure has become the major treatment method for BCS with inferior vena cava thrombosis instead of open surgery. Therefore, to investigate the effectiveness and safety of this method, here we compared the 2 methods (open procedure and PTA) that had been used in our clinic to help others select the ideal treatment method.
MATERIALS AND METHODS Patients This is a retrospective analysis of data from patients with BCS with inferior vena cava thrombosis treated at the Department of Vascular Surgery of the First Affiliated Hospital of Bengbu Medical College between January 1997 and December 2017. The inclusion criteria were: (1) patients with confirmed diagnosis of BCS accompanied with inferior vena cava thrombosis by clinical manifestations and imaging examinations on admission (Fig. 1A, E, F); (2) patients’ liver functions were slightly abnormal, and the examinations of the cardiac and pulmonary functions suggested that they could tolerate the operation; and (3) the patients received either an open surgical procedure or preopening and PTA. This study has been approved by the Ethics Committee of our hospital. Study Design For the patients in the open group (n ¼ 32), conventional open surgery, namely resection of the lesions in inferior vena cava, removing thrombus, and consequent revascularization were conducted under direct vision. For the patients in the PTA group (n ¼ 56), preopening and staged PTA of the inferior vena cava were conducted. The patients in the open group received the open procedure during the earlier time period (from January 1997 to December 2010) and had both new or old thrombi in the inferior vena cava, while the patients in the PTA group who received interventional therapy later (from January 2010 to December 2017) mainly had a new thrombus in the inferior vena cava, with lesions in the partial segment of the inferior vena cava. There was 1 year (2010) during which the open procedures were gradually replaced by preopening and staged PTA of the inferior vena cava.
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Fig. 1. Open radical treatment. (A) Inferior vena cava venography shows BCS accompanied with inferior vena cava thrombosis; (B) thrombus can be seen after resecting the inferior vena cava; (C) the lesion and thrombus in the inferior vena cava; (D) suturing the wound of the inferior vena cava; (E, F) varicosity on the thoracic and abdominal walls, as well as swollen belly of the patient before operation; and (G, H) varicosity on the thoracic and abdominal walls, as well as swollen belly of the patient disappeared after the operation. For the interventional therapy, namely preopening and staged PTA of the inferior vena cava in this study (Fig. 2), the patients were treated in the interventional treatment room under local anesthesia. Catheterization via the femoral vein or bidirectional catheterization via the femoral and jugular veins was conducted. First, DSA of the inferior vena cava was conducted after catheterization to further confirm the lesions and thrombus in the inferior vena cava. For the cases with partial segment blockage, bidirectional venography was needed to clarify the length and angle of the lesion in the inferior vena cava, and a super-hard guidewire was used for the puncture via the cervical and/or femoral vein. A small balloon with a diameter of about 6e10 mm was selected according to the size and time of formation of the thrombus to dilate the involved segment for PTA and preopening (Fig. 2A). The process only involved a single dilation of the blood vessel, which avoided the damage of multiple
dilations on the thrombus in the inferior vena cava, and therefore reduced the risk of drop-off. Venography showed that blood could flow through the inferior vena cava, while the thrombus was evidently not moved. A pigtail catheter was inserted for thrombolysis (600,000e 800,000 units of urokinase, injected into the catheter in 2e3 times) for 3e5 days (Fig. 3A). During the postoperative hospital stay (5e7 days), subcutaneous injection of low molecular weight heparin (5,000 units, every 12 hr) for anticoagulation was performed, which was changed to oral intake of warfarin before discharge (the dose was adjusted according to the prothrombin time and international nomalized ratio monitoring results). The patients were hospitalized again 1 month later, and interventional therapy was conducted after sufficient preparation. During the operation, an appropriate caliber balloon was selected according to the situation of thrombolysis in the inferior vena cava, as shown in venography, to dilate the involved segment (Fig. 2B). Staged interventional therapy was conducted every 1e3 months; until the thrombus in the inferior vena cava had completely disappeared, a 20- to 25-mm diameter balloon was used to dilate the lesion area until satisfactory effects were obtained (Figs. 2C and 3B) (namely, stenosis of the inferior vena cava was 30%), and then oral intake of warfarin was continued for 6 months to 2 years after successful therapy.
Treatment Methods
vena cava was conducted, and a balloon Foley catheter was used to block the distal end of the inferior vena cava. The lesion in the inferior vena cava was resected and the thrombus in the inferior vena cava was completely removed under direct vision (Fig. 1B, C). According to the disease conditions at the inferior vena cava, direct suturing (diaphragm), patching expansion revascularization (Fig. 1D) (diaphragm or partial segment blockage), or orthotopic
Open operation was conducted under inhalation general anesthesia. An incision was made on the left chest, the pericardium and part of the diaphragm were resected, and the retrohepatic segment of the inferior vena cava (RHSIVC) and the right atrial portal vein were fully dissected. Cuff-blocking of the proximal end of the inferior
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Annals of Vascular Surgery
Fig. 2. Treatment of a case in the PTA group. (A) An 8mm balloon was used for predilation (a, venography of the inferior vena cava shows BCS accompanied with inferior vena cava thrombosis; b, an 8-mm balloon was used to dilate the lesion area; c, venography after operation showed that blood flowed through the lesion area, while the shape of thrombus had not changed). (B) A 10-mm balloon was used for dilation (a, venography of the inferior vena cava showed that most of the thrombus had disappeared; b, the 10-mm balloon was used to dilate
the lesion again; c, venography showed that blood flowed satisfactorily in the inferior vena cava, and the shape of the thrombus is not changed). (C) An 18-mm balloon was used for dilation (a, venography of the inferior vena cava showed that the thrombus had disappeared; b, an 18-mm balloon was used for dilation again; and c, postoperative venography showed that blood flow in the inferior vena cava was generally smooth).
artificial blood vessel transplantation (partial segment blockage) was conducted. An autologous blood transfusion device was used to retransfuse the surgical bleeding during surgery. The varicose vessels at the surgical incision were treated by ligation and electrocoagulation for hemostasis.
compliance of the patients. Then the follow-up was changed to every 6 months during the second year after operation, and the last follow-up was generally 60 months after operation, which varied according to the compliance of the patients. Color Doppler ultrasonography was generally used for follow-up examinations, but computed tomographic venography (CTV) was used for some patients. In addition, other indexes were also collected during follow-up: liver function, high pressure of the inferior vena cava, ascites, thrombus
Follow-up In the first year after operation, the patients were followed every 1e3 months, according to the
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Fig. 3. Treatment of a second case in the PTA group. (A) An 8-mm balloon was used for predilation (a, venography of the inferior vena cava showed BCS accompanied with inferior vena cava thrombosis; b, an 8-mm balloon was used to dilate the lesion; and c, pigtail catheter was inserted for thrombolysis, venography showed that blood flowed through the inferior vena cava, and
the shape of the thrombus changed slightly). (B) A 20mm balloon was used for dilation (a, venography showed that the thrombus in the inferior vena cava had completely disappeared; b, a 20-mm balloon was used for dilation again; and c, venography after operation showed that blood flowed smoothly in the inferior vena cava).
in the inferior vena cava, and stenosis rate of the lesion area in the inferior vena cava.
patients, 59 had membranous obstruction of the inferior vena cava accompanied with thrombus, and 29 had short segment blockage of the inferior vena cava accompanied with thrombus. The clinical manifestations of the patients mainly included abdominal distension, varicosity on the thoracic and abdominal walls, splenomegaly, ascites (62 patients), edema of both lower extremities, and superficial varicosis. Some patients also presented with hyperpigmentation or ulcers. Seventeen patients had a history of upper gastrointestinal hemorrhage before hospitalization, which mainly manifested as hematemesis or melena. In addition, 59.09% (52/ 88) of the patients had been treated in other hospitals for liver cirrhosis or ascites. Color Doppler ultrasonography of blood vessels showed membranous obstruction of the RHSIVC or partial segment blockage of inferior vena cava, while the distal lumen of the blood vessel showed solid echo, with part of limited movement. CTV of the inferior vena cava of 50 patients showed
Statistical Analysis SPSS 19.0 (IBM Corp., USA) was used for statistical analysis. Quantitative data were described with means and standard divisions, and t-test was used for the comparison. Qualitative data were compared with chi-squared test. P < 0.05 was considered statistically significant.
RESULTS Baseline Characteristics Totally, 88 patients (including 47 males and 41 females) were included in this study (Table I). The mean age of the patients was 41.82 ± 10.12 years (range 29e65), and the mean disease duration was 10.28 ± 5.66 months (range 2e24). Among these
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Table I. General characteristics of the patients included in the study
n Male/female Age (years) Membranous obstruction type, n Partial segment blockage type, n Disease duration (months) Ascites, n Hepatomegaly, n Splenomegaly, n Upper gastrointestinal hemorrhage, n Edema of both lower extremities, n Varicosity of both lower extremities, n
Open group
PTA group
P-value
32 17/15 40.68 ± 10.95 20 12 10.85 ± 5.27 22 8 30 6 32 26
56 30/26 41.85 ± 10.06 39 17 11.02 ± 6.15 40 17 53 11 56 42
0.9678 0.6126 0.4929 0.4929 0.8959 0.7911 0.5919 0.7607 0.9187 1.0000 0.5009
membranous obstruction of the RHSIVC or partial segment blockage of inferior vena cava (length 25e50 mm, mean length 40.12 mm), and the distal part of the inferior vena cava had filling defects of different sizes and shapes. Normal images of the hepatic vein were found in 43 patients, while the others showed evidence of an accessory hepatic vein. Routine catheterization of the inferior vena cava was conducted before interventional therapy for digital subtraction angiography (DSA) and venography of the inferior vena cava, which showed dilation of the segment distal to the blockade in 38 patients, with large filling defects and no evident movement. Attachment and contrast agent retention were found in most patients. The findings in venography of the hepatic vein were similar to the findings in CTV. Perioperative Characteristics The procedures in the open group were all successful, with a mean operation time of 7.56 ± 0.25 hr, and mean intraoperative blood loss volume of 6,500.89 ± 150.20 mL (Table II). All the blood was transfused back to the patient via extracorporeal circulation. No pulmonary embolism was found during and after the operation, and the technical success rate was 100%. One patient in this group died of intrathoracic bleeding after the operation. In the PTA group, 2 patients experienced thrombus shifting that blocked the preopened blood flow by venography during the second treatment. One of these patients could not receive interventional therapy due to enlargement of the thrombus in the inferior vena cava and was considered to have treatment failure, and the other patient had restored blood flow after dilation with a 12-mm balloon. The treatments in all the other patients were successful, and the treatment success rate was 98.21% (55/56). The
total treatment times in this group were 3e6 times for each patient, with a mean treatment times of 4.15. None of the patients received stenting after PTA. The mean treatment time of a single intervention was 2.15 ± 0.25 hr, and the mean blood loss volume was 50.65 ± 5.92 mL. Inferior vena cava hypertension alleviated after the operation, ascites disappeared gradually, and liver function (indicated by total bilirubin, serum prealbumin, and albumin levels) improved. The mean hospital stay was 14.18 ± 1.36 and 5.87 ± 1.02 days for the patients in the open group and PTA group, respectively. Follow-up All patients were followed regularly, with mean follow-up time of 32 months (range 3e60). Color Doppler ultrasonography of the inferior vena cava was used to assess the degree of restenosis, which showed that 2 patients in the open group had stenosis of the inferior vena cava evident 2 years after operation, which was then treated with balloon dilation and angioplasty. Thus, the recurrence rate in the open group was 6.25% (2/32). In the PTA group, 7 patients had severe restenosis (stenosis rate >50%) at 18e42 months after operation, and the recurrence rate was 12.96% (7/54). No new thrombosis was found in the PTA group. Interventional therapy was further conducted for balloon dilation in these 7 patients, which successfully restored the normal blood flow in the inferior vena cava.
DISCUSSION In this study, we retrospectively analyzed the data of 2 groups of patients with BCS with thrombus in
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Table II. Comparison of perioperative data between the 2 groups
n Operation time (hr)a Intraoperative blood loss (mL) Operative death, n Technical success rate (%) Single hospital stay (days)a Postoperative recurrence rate (%) a
Open group
PTA group
P-value
32 7.56 ± 0.25 6,500.89 ± 150.20 1 100 14.18 ± 1.36 6.25
56 2.15 ± 0.25 50.65 ± 5.92 0 98.21 5.87 ± 1.02 12.96
<0.00010 <0.0001 0.7756 0.7756 <0.0001 0.5720
For each interventional session (i.e., 1 session in the open group and 3e6 sessions in the PTA group).
the inferior vena cava that was treated at our center by open or PTA methods to investigate the effectiveness and safety of these treatments. The results showed that the conventional radical open operation had several disadvantages, including complex operation procedures, long operation time, large volume of intraoperative blood loss, and various postoperative complications. In contrast, preopening of the inferior vena cava and staged PTA had evident clinical advantages, which were more pronounced regarding safety, minimal invasion, and rapid recovery. In addition, the PTA method could be used on a wider range of patients including those with indications that suggested they could not tolerate an open operation. The effectiveness of the PTA method used in this study was as high as 98.2% in the 56 patients included in the PTA group, which compares well with other studies. Meng et al.20 found that they achieved effective treatment in 96.4% of 55 similar patients using balloon dilation with stent placement and thrombus aspiration. Another study used recoverable stents with agitation thrombolysis or catheter-directed thrombolysis of the inferior vena cava in 40 patients and achieved 100% success; however, the stents were removed successfully in only 92.1% of patients and there was a case of acute pulmonary embolism.21 While a small study on 17 patients suggested 100% effectiveness with combined thrombus aspiration and inferior vena cava recanalization.22 Therefore, these studies support our data that suggest that interventional therapy is a suitable approach for treating patients with BCS with inferior vena cava thrombosis and methods not involving stents may be preferable. Preopening of the inferior vena cava to provide a small lumen restored the blood flow in the inferior vena cava to a degree, which could change the vortex of blood flow to forward blood flow. The anticoagulation and direct thrombolysis that accompanied the procedure also induced lysis of the thrombus. The overall structure of the thrombus was not
damaged during the treatment, and the blood flow in a 6- to 10-mm wide inferior vena cava not only insured the patency and forward direction of blood flow, but also avoided thrombus shifting from too strong a blood flow to block the newly formed lumen (this occurred in only 2 patients in this study, resulting in treatment failure in one of them). The risk of the thrombus falling off into the right atrium to induce pulmonary embolism was also avoided. In staged PTA, balloons with different diameters were selected according to the thrombolysis situation in the inferior vena cava, and therefore gradually opened the vein to restore normal blood flow. The authors speculate that a newly formed thrombus could be rapidly lysed, but the relatively high risk of shifting should also be considered. Therefore, we suggest caution when choosing the balloons, those with large diameters should not be selected. In contrast, an old thrombus has generally adhered to the blood vessel wall and is unlikely to fall off, although the lysis of the thrombus is relatively slow. Nevertheless, choosing balloons for such cases is more flexible, and we think that the diameter of the balloon should be about half of the diameter of the thrombus. Ensuring the safety of interventional therapy during the first predilation of the inferior vena cava provided a basis for the successful staged dilation. Staged PTA was very safe and easy to perform. Although the overall treatment duration was relatively long, every single hospital stay was very short. In addition, the success rate of the treatment was very high, and the clinical effectiveness was definite. In this study, 55 of the 56 patients were successfully treated, and the success rate was as high as 98.21%. There are several issues we should consider during interventional therapy. First, the first preopening of inferior vena cava is the key process in treating BCS accompanied with inferior vena cava thrombosis. Such preopening is relatively easy for the patients with membranous obstruction, but harder for those with partial segment blockage,
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because of different anatomic angles (lefteright or anterioreposterior angles). Therefore, opening in the patients with partial segment blockage of inferior vena cava could easily create a false lumen, and dilation could lead to serious outcomes such as pericardial tamponade or major hemorrhage. We suggest that the following should be considered: (1) sufficiently review of the CTV images before operation to clarify the anatomic angles of the inferior vena cava, which could provide evidence for the selection of appropriate angle for puncture in interventional therapy; (2) according to the preoperative assessment, the ‘‘C’’ shaped branch of DSA should be rotated appropriately; and (3) bidirectional puncture should be conducted, with a pigtail catheter inserted in the contrary end, and the proximal end should be used for guidance, which could increase the puncture success rate and the accuracy of the chosen direction. In order to ensure the safety and effectiveness of staged dilation, the following should also be considered: (1) a 1-month interval between 2 dilations is best for the patients, as a shorter interval prevents thrombolysis, and a longer interval could lead to reobstruction of the opened blood vessel; (2) the shape and structure of the thrombus should not be damaged to avoid partial fall of the thrombus; and (3) the interval between the staged dilation could be selected according to the results of the color Doppler ultrasonography of the inferior vena cava. Each dilation must not be conducted too quickly; we only dilate the lesion to a normal anatomic caliber after the thrombus in the inferior vena cava has completely disappeared; and (4) the treatment duration should be sufficient, and the postoperative anticoagulation must be adequate, which assists thrombosis and prevents postoperative recurrence of thrombosis. There are several limitations in this study. First, this is a retrospective study and the data of the 2 groups were from different time periods because the interventional therapy needed to be developed before we could use it for vascular disorders. This time difference is likely to have introduced some bias into patient grouping. In addition, the overlap of the 2 methods in 2010 could have introduced additional bias. Second, as the data were retrospective, the data were not always complete and homogeneous between groups. Although the investigators tried different methods in analyzing the data, we still could not ensure standardization of the treatment methods, or the homogeneity of the observational endpoints, which could lead to bias in the assessment of treatment effectiveness and safety profiles.
Annals of Vascular Surgery
CONCLUSIONS Preopening and staged PTA of inferior vena cava is a safe and simple method for the treatment of BCS accompanied with inferior vena cava thrombus, which had satisfactory clinical effectiveness and is applicable in clinical practice. REFERENCES 1. Hefaiedh R, Cheikh M, Marsaoui L, et al. The Budd-Chiari syndrome. Tunis Med 2013;91:376e81. 2. Valla DC. Primary Budd-Chiari syndrome. J Hepatol 2009;50:195e203. 3. Ferral H, Behrens G, Lopera J. Budd-Chiari syndrome. AJR Am J Roentgenol 2012;199:737e45. 4. Dang XW, Xu PQ, Ma XX, et al. Surgical treatment of BuddChiari syndrome: analysis of 221 cases. Hepatobiliary Pancreat Dis Int 2011;10:435e8. 5. Qi XS, Ren WR, Fan DM, et al. Selection of treatment modalities for Budd-Chiari Syndrome in China: a preliminary survey of published literature. World J Gastroenterol 2014;20:10628e36. 6. Seijo S, Plessier A, Hoekstra J, et al. Good long-term outcome of Budd-Chiari syndrome with a step-wise management. Hepatology 2013;57:1962e8. 7. Clark PJ, Slaughter RE, Radford DJ. Systemic thrombolysis for acute, severe Budd-Chiari syndrome. J Thromb Thrombolysis 2012;34:410e5. 8. Zhang F, Wang C, Li Y. The outcomes of interventional treatment for Budd-Chiari syndrome: systematic review and meta-analysis. Abdom Imaging 2015;40:601e8. 9. Meng QY, Sun NF, Wang JX, et al. Endovascular treatment of Budd-Chiari syndrome. Chin Med J (Engl) 2011;124: 3289e92. 10. Lei AW, Ruizhao Q, Zhendong Y, et al. Method and safety analysis of interventional treatment of Budd-Chiari syndrome in 1246 patients. Chin J Digestive Surg 2016;15:702e8. 11. Shen Q, Xue HZ, Jiang QF, et al. Surgical treatment of BuddChiari syndrome with hepatic inferior vena cava occlusion and thrombosis by interposition graft caval-atrial shunt. Chin J Hepatobiliary Surg 2011;17:334e6. 12. Ding PX, Li YD, Han XW, et al. Treatment of Budd-Chiari syndrome with urokinase following predilation in patients with old inferior vena cava thrombosis. Radiol Med 2011;116:56e60. 13. Zhang QQ, Xu H, Zu MH, et al. Strategy and long-term outcomes of endovascular treatment for Budd-Chiari syndrome complicated by inferior vena caval thrombosis. Eur J Vasc Endovasc Surg 2014;47:550e7. 14. Li XQ, Wu YM, Zhou WM, et al. The diagnosis and treatment of Budd-Chiari syndrome with inferior vena cava thrombosis. Chin J Gen Surg 2002;17:27e8. 15. Han XW, Ding PX, Li YD, et al. Retrieval stent filter: treatment of Budd Chiari syndrome complicated with inferior vena cava thrombosisdinitial clinical experience. Ann Thorac Surg 2007;83:655e60. 16. Ren JZ, Huang GH, Ding PX, et al. Outcomes of thrombolysis with and without predilation of the inferior vena cava (IVC) in patients with Budd-Chiari syndrome with old IVC thrombosis. Vasc Endovascular Surg 2013;47:232e8. 17. Liu L, Qi XS, Zhao Y, et al. Budd-Chiari syndrome: current perspectives and controversies. Eur Rev Med Pharmacol Sci 2016;20:3273e81.
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18. Wang YL, Ding PX, Li YD, et al. Comparative study of predilation with stent filter for Budd-Chiari syndrome with old IVC thrombosis: a nonrandomized prospective trial. Eur J Radiol 2012;81:1158e64. 19. Gao Y, Chen S, Yu C. Applicability of different endovascular methods for treatment of refractory Budd-Chiari syndrome. Cell Biochem Biophys 2011;61:453e60. 20. Meng X, Lv Y, Zhang B, et al. Endovascular management of Budd-Chiari syndrome with inferior vena cava thrombosis:
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a 14-year single-center retrospective report of 55 patients. J Vasc Interv Radiol 2016;27:1592e603. 21. Bi Y, Chen H, Ding P, et al. Long-term outcome of recoverable stents for Budd-Chiari syndrome complicated with inferior vena cava thrombosis. Sci Rep 2018;8:7393. 22. Fu YF, Xu H, Wu Q, et al. Combined thrombus aspiration and recanalization in treating Budd-Chiari syndrome with inferior vena cava thrombosis. Radiol Med 2015;120: 1094e9.