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REVIEW ARTICLE |
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| Year : 2014 | Volume
: 19
| Issue : 4 | Page : 195-200 |
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Wilms' tumor with intravascular extension: A review article
Suzanne McMahon, Robert Carachi
Department of Surgical Paediatrics, Royal Hospital for Sick Children, Glasgow, United Kingdom
| Date of Web Publication | 30-Sep-2014 |
Correspondence Address:
Suzanne McMahon
Department of Surgical Paediatrics, Royal Hospital for Sick Children, Dalnair Street, Glasgow, G3 8SJ
United Kingdom
 Source of Support: None, Conflict of Interest: None  | Check |
DOI: 10.4103/0971-9261.141998
 Abstract | | |
Intravascular extension of Wilms' tumor is a well-recognized phenomenon. Intravascular extension into the vena cava occurs in only 4-8% of patients with Wilms' tumors and intraatrial extension occurs in around 1-3% of patients. This review of the published literature in this cohort aims to summarize the findings of different case series to provide an optimum management plan. A literature search was performed and index papers were retrieved for review. The search included the following terms: Intracaval, intravascular, intraatrial and intracardiac extension of Wilms' tumor or nephroblastoma. The management of patients with intravascular tumor thrombus in Wilms' tumor is complex. A skilled multi-disciplinary team at a tertiary referral center with cardiothoracic surgery available should manage these patients. Multi-modal diagnostic and preoperative imaging are required to confirm and define the extent of the extension. Preoperative chemotherapy is advocated for all but exceptional circumstances and must be followed closely. Surgical resection should be planned according to the stage of intravascular extension with possible need for cardiopulmonary bypass and deep hypothermia with cardiac arrest if required. Surgical complications are more common in this group of patients, but outcome is comparable to those without intravascular extension, and is more closely correlated with the histological subtype then stage of intravascular extension. Operative imaging are required to confirm and define the extent of the extension.
Keywords: Intravascular extension, management, Wilms′ tumor
How to cite this article:
McMahon S, Carachi R. Wilms' tumor with intravascular extension: A review article
. J Indian Assoc Pediatr Surg 2014;19:195-200 |
| Introduction | |  |
Intravascular extension of Wilms' tumor is a well-recognized phenomenon. Intravascular extension into the vena cava occurs in only 4-8% of patients with Wilms' tumor and intra-atrial extension occurs in around 1-3% of patients. [1],[2]
Intravascular extension is more common in right-sided Wilms' tumor due to the shorter right-sided renal vein. It is also recognized to be more common in older children with Wilms' tumor, with a mean age of 3.75 years versus 2.97 years without intravascular extension. [1] Difficulty then arises in trying to compare the outcomes for patients with intravascular extension versus those without, as we know that increasing age is a poor prognostic factor in this condition. [1]
Cavo-atrial extension is much less frequent and, indeed, prolapse of the tumor through the tricuspid valve and into the right ventricle can occur [2] [Figure 1]. Intracardiac tumor thrombus is often asymptomatic and may have absent clinical signs. [3],[4] | Figure 1: Echocardiogram showing intraatrial extension of tumor thrombus prolapsing into the right ventricle
Click here to view |
Dramatic advances in the management of Wilms' tumor have recently seen more than 85% of patients with localized disease being completely cured and 70% surviving metastatic disease. [5] Survival nowadays is the result of well-organized and coordinated trials both on a nationwide and an international basis and the use of multi-modal therapy. In 1969, the National Wilms' Tumor Study Group (NWTS) was formed, joining North America in the fight against Wilms' tumor. Shortly thereafter, in 1971, the Societe Internationale D'oncologie Pediatrique (SIOP) formed an equivalent European group. In 1977, the United Kingdom Children's' Cancer Study Group (UKCCSG) was formed, contributing further to the research, joining in 2006 with the UK Childhood Leukaemia Group to become the Children's Cancer and Leukaemia Group (CCLG). In 2000, the Children's Oncology Group (COG) was formed as a worldwide clinical trial cooperative study group for Wilms' as well as for other tumors. [5] These main collaboratives have differences both in their staging criteria and in their management.
| Preoperative identification of intravascular thrombus | | |
The diagnosis of intravascular thrombus and its level was achieved in patients in the SIOP 93-01/GPOH and the SIOP 2001/GPOH studies using a combination of modalities. Ultrasound with Doppler was the most commonly used (94%), and has been proven to be effective and reliable and has the benefit of being able to be used intraoperatively if required. [6],[7],[8],[9] The second most popular imaging modality used was computed tomography (CT) (76%), which is routinely used in the staging of patients with Wilms', although the sensitivity to identifying tumor thrombus is noted to be less as is the accuracy of determining the level of thrombus extension [6] [Figure 2] and [Figure 3]. Twelve percent of the group had venography, where the level of extension of the tumor thrombus remained unclear. The use of venacavography has generally been advocated only in attempt to define the upper limit of a thrombus that is indeterminable by other methods. The difficulty in performing this investigation routinely lies in its interpretation. When the child cries or when there is compression of the vena cava, the blood is diverted through the paravertebral veins and can mimic intracaval extension. [10]
Although magnetic resonance imaging has been described by some papers as the optimum method for visualizing intravascular extension of tumor thrombus, [6],[11] it was used in only 41% of the study group and in only two of the 29 patients described by Mushtaq et al. with only 50% sensitivity. [12] Its use will need to be further evaluated to justify its role in this scenario. | Figure 2: Computed tomography scan showing large, right-sided Wilm's tumor with thrombus extending into the IVC
Click here to view |
 | Figure 3: Computed tomography scan showing another large, right-sided Wilm's tumor with thrombus extending into the IVC
Click here to view |
Khanna et al. showed in 2012 that both the sensitivity and the specificity of preoperative determination of intravascular extension of tumor thrombus is increased after chemotherapy, both in CT and Doppler ultrasound. CT sensitivity increased from 65.6% to 86.7% in the primary nephrectomy group versus the secondary nephrectomy group and Doppler sensitivity increased from 45.8% to 66.7%. Similarly, the specificity increased in the CT group from 84.8% to 90.6% and the Doppler ultrasound increased from 95.7% to 100%. Similar improvements were seen in the identification of atrial extension for CT but not for Doppler. [13]
This further supports the SIOP and CCLG protocols for the preoperative administration of chemotherapy to facilitate accurate radiological staging, which alters the surgical approach.
In 1991, Ritchey et al. showed the use of echo to be highly sensitive at identifying intraatrial extension, demonstrating it in 14 of their 15 patients. [14] Indeed it is suggested that all patients identified as having intravascular extension should have echo performed, as patients with intracardiac extension are often asymptomatic. [2],[12]
By combining the imaging methods mentioned above, Szavay et al. successfully identified all of their patients prior to treatment. [6]
Although we have highlighted the importance of preoperative imaging, it should be emphasized that detailed clinical examination should not be forgotten in the advent of advancing technology. The presence of a varicocele can highlight intravascular extension, as can hepatomegaly and ascites; therefore, a thorough clinical examination should be performed in all patients with Wilms' tumor. [1],[15]
| Staging of intravascular thrombus | | |
The degree of intravascular extension is often variable and the operative techniques and difficulties can differ in accordance with the state of the disease.
Several staging classifications have been suggested in the past for tumors other than Wilms' tumor, extending into the inferior vena cava (IVC) or atrium. In 1982, Cummings suggested a classification system of renal cell carcinoma (RCC) based on the location of the tumor thrombus relative to the diaphragm. [10],[16] Subsequently, in 1986, Pritchett et al. went on to describe thrombus extension relative to the hepatic vessels in the IVC defining three levels - Level I: Infrahepatic intravascular extension, Level II: Intrahepatic extension and Level III: Suprahepatic or atrial extension of intravascular thrombus. [17] Shortly thereafter, in 1987, Staehler et al. described a more detailed four-stage system that was modified by Daum in 1994, which considered the extent of intimal attachment of the thrombus. [10] He described Stage I as a small <5 cm thrombus extension into the IVC below the level of the hepatic vessels; Stage II a large thrombus >5 cm but still below the hepatic vessels; Stage III as extending to the level of the hepatic vessels and above providing more operative difficulty obtaining proximal control; and Stage IV as tumor thrombus extending to the atrium.
Although these classifications systems have evolved in the adult population, the intraoperative difficulties encountered in Wilms' tumor in children are similar. In 2013, Abdullah et al. suggested a modification of Daum's classification above establishing a very comprehensive tool. They suggest the addition of Stage V for intraventricular extension of tumor thrombus having encountered this in two of their nine patients with intracardiac extension. The importance of preoperatively establishing this lies in the anesthetic approach. Positive pressure ventilation may cause tricuspid valve obstruction and immediate loss of cardiac output. [2]
In Stage V, the authors suggest that the respective stage be allocated a, b or c at the time of surgery to indicate the degree of intimal involvement. a indicates that the thrombus is free from the vessel wall, b denotes that the thrombus is adherent to the vessel wall or vessel wall infiltration and c indicates hepatic vein involvement (which could therefore by definition only be added to Stages 3-5) [2] [Table 1]. | Table 1: Abdullah's modification of the intracaval thrombus staging classification[2]
Click here to view |
The use of such a staging system depends heavily on the accurate preoperative determination of thrombus location. It is accepted that the degree of attachment to the intima will often be an intraoperative finding; however, the use of such a tool is still helpful in the preoperative planning of surgical strategy.
Having accurate preoperative imaging to determine the degree of intravascular extension would facilitate the planning of the preferred operative strategy in order to reduce the surgical complication rate in this complex cohort.
| Management based on intravascular extension | | |
Neoadjuvant chemotherapy
Despite the different management protocols between the three main collaboratives after the NWTS 5 study, all the bodies agreed that the identification of intravascular tumor thrombus into the IVC above the levels of the hepatic veins should ideally be treated with preoperative chemotherapy. [5],[12] Chemotherapy also has the advantage of treating metastasis concurrently in disseminated disease. There are exceptions to this, which will be discussed below.
It has been shown in various studies that a significant number of tumors will regress on preoperative chemotherapy prior to resection, facilitating an easier surgery with less likelihood of complication and potentially negating the need in some instances for the use of cardiopulmonary bypass (CPB). [12] Szavay et al. demonstrated the regression of more than 25% of the tumor in 65% of their patients [6] and Abdullah observed the complete disappearance of atrial tumors in 20% of his series. [2] Lall et al. found a significant shrinkage of the thrombus and tumor in the majority of their case series on their preoperative imaging and avoided the need for cavotomy at the time of delayed nephrectomy in nearly half of their patients. [1] Shamberger et al. found regression of the intravascular thrombus in 39 of the 49 patients with comparable pre - and postchemotherapy imaging. They also found that seven of 12 patients with intraatrial extension had regressed far enough to negate the need for CPB. [15] Although it provides an established and prepared approach to very high-risk surgical resections that might not otherwise be considered resectable, CPB is not without significant risk in its own right. [18]
Chemotherapy regimens are again protocol driven, with NWTSG advocating the use of vincristine, dactinomycin and doxorubicin. [5] SIOP guidance prefers the use of actinomycin D and vincristin, adding in adriamycin if metastases are present. [6] Preoperative chemotherapy also carries risk and Shamberger et al. found that five of 69 patients receiving neoadjuvant chemotherapy had complications-one tumor embolus, one case of tumor progression and three cases of acute respiratory distress syndrome, of which one was fatal. [15]
Neoadjuvant chemotherapy in this group requires close surveillance for evidence of tumor regression. Failure of regression may mandate early resection. Elective surgical resection should be planned based on evidence of tumor response to chemotherapy with regard to the extent of thrombus, volume and appearance of the thrombus and presence of atrial extension on imaging. [19] Chemotherapy should be continued until the tumor is considered resectable by the treating surgical team. Shamberger et al. found a median treatment duration of 8 weeks, Szavay et al. described a 4 week administration while Murthi et al. described the use of neoadjuvant chemotherapy for up to 29 weeks. [15],[6],[19]
It is widely accepted now that preoperative preparedness is the key to reducing perioperative complications and mortalities in this complex group. As such, surgery for patients with preoperative diagnosis of atrial involvement or indeed proximal extension requiring the potential for CPB should be performed at a center with both pediatric and cardiac surgeons. [10]
Surgical technique based on stage
The operative resection of Wilms' tumor with intravascular extension represents a significant challenge, and the surgeons involved should have an appropriate level of experience. Imaging should be repeated preoperatively and the tumor thrombus extension should be restaged.
The renal tumor with extension below the hepatics can be approached via a rooftop incision or transverse upper abdominal incision. Proximal extension above the hepatics (stages III and above) necessitate the same incision extended to median sternotomy or an inverted "Y". [19]
Stage I
The vena cava is mobilized and clamped above and below the renal veins as well as the contralateral renal vein. Care is taken to apply these above and below the limits of the thrombus to avoid tumor embolus. At the insertion of the renal vein, longitudinal cavotomy is performed and a stage Ia thrombus can be excised. Stage Ib thrombi will require partial resection and patch closure. [10]
Stage II
As for Stage I, although more proximal isolation of the vena cava will be required.
Stages III, IV and V
The diaphragm is divided anteriorly in the midline and the liver is rotated to expose the IVC in its entirety. After systemic heparinization, the ascending aorta, right atrium and superior vena cava (SVC) are cannulated with Ch14-16 cannulae. The right femoral vein or IVC is then cannulated (Ch6). The pulmonary artery is slinged to prevent pulmonary tumor embolus. At this stage, moderate to deep hypothermia can be induced using cold Ringers and Mannitol solution to bring the patient's core (nasopharyngeal) temperature to 16-20 o C. Cardiac arrest or aortic cross-clamping can then be used. Cardiac arrest can be extended to 40 min during hypothermia with reduced morbidity. [10],[19] The IVC is incised to the level of the involved renal vein, which is circumferentially incised to visualize the thrombus, which is then dissected free using both blunt instrumental and digital dissection and the thrombus is excised. Because of intimal involvement (I-Vb), it is not always possible to remove en bloc and may require to be removed piecemeal. Extension inferiorly and or into the contralateral vein should be dissected and excised similarly. Primary repair of the IVC with Prolene is performed if possible. After extensive dissection, bovine or autologous pericardial graft may be required to restore adequate IVC caliber. If the IVC has been completely occluded, surgery may involve cavectomy in continuity with the tumor up to the level of tumor clearance. [2] Thrombus may be adherent to the intima, requiring venous resection and venoplasty. [2] Hemostasis should be achieved and hypothermia reversed. Pericardial and pleural drains are placed and the abdomen and chest are closed. Drains are removed after 24-48 h. [19]
In Stage V extension, the child is anesthetized but maintained on spontaneous ventilation while all the lines were inserted and the patient prepped and draped ready for median sternotomy and cannulation for CPB prior to laparotomy for tumor resection. [2]
Long-term aspirin is prescribed to patients with grafts.
| Indications for primary resection | | |
All three collaboratives (SIOP, NWTRG and CCLG) advocate the preoperative use of chemotherapy when intravascular extension is identified. [20] However, there are specific clinical scenarios that do not allow for the safe administration of the neoadjuvant therapy advised. In these instances, the balance of risk favors the elective (usually urgent) primary resection of the tumor and thrombus by both an experienced pediatric surgeon and cardiothoracic surgeon with CPB available.
Murthi et al. had a case of unstable tumor thrombus on a narrow pedicle identified on echo. Primary resection was performed to avoid the risk of potentially fatal tumor embolus. [19] Szavay et al. describe the acute presentation of a child with traumatic tumor rupture requiring primary resection. [6] Both Abdullah and Mushtaq have referenced encounters with a child with Budd Chiari syndrome in their series. Both have advocated primary resection with CPB. [2],[12]
As previously mentioned, patients with intravascular tumor extension must be closely monitored during neoadjuvant therapy. In the event that no tumor response or even tumor progression is observed, chemotherapy should be interrupted and primary resection will be required with CPB and cardiothoracic surgical support. [21]
Neoadjuvant chemotherapy itself is not without risk, providing its own mortality rate. Failure to tolerate chemotherapy may necessitate primary resection.
| Outcome | | |
Neither the level of tumor thrombus nor the use of CPB was predictive of survival. [6]
There is however an increase in the incidence of surgical complications in patients with intravascular extension, [3],[14],[19] with an odds ratio of 2.2 if intravascular extension is present. There was an association between lower surgical complication rate and the administration of neoadjuvant chemotherapy. [15]
Most papers denote that the single best predictor of survival is the histological subtype. [4],[6],[9],[15] There is no association between unfavorable histological and propensity to have intravascular tumor thrombus. [15]
There is no significant difference in survival outcomes in comparison with children without intravascular extension. [4]
Index case series are highlighted in [Table 2].  | Table 2: Outcome of patients with various degrees of intravascular extension
Click here to view |
| Conclusion | | |
The surgical resection of Wilms' tumor with intravascular extension remains a formidable challenge. Intravascular and intracardiac extension must be excluded in all patients with Wilms' tumor. [2] With accurate identification of this problem, subsequent preoperative chemotherapy and resection with an appropriately skilled team, the survival rates are not significantly different from those with uncomplicated Wilms' tumor. [6]
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[Figure 1], [Figure 2], [Figure 3]
[Table 1], [Table 2]
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