Surgical resection of a renal cell carcinoma involving the inferior vena cava: the role of the cardiothoracic surgeon
Journal of Cardiothoracic Surgery
Surgical resection of a renal cell carcinoma involving the inferior vena cava: the role of the cardiothoracic surgeon
Haralabos Parissis 0
Mohammad Taukeer Akbar 2
Michael Tolan 1
Vincent Young 1
0 Royal Victoria Hospital , Grosvernor Rd, Belfast, BT12 6BA , Northern Ireland
1 Cardiothoracic Department, St James Hospital , Dublin , Ireland
2 Essex Cardiothoracic Center, Basildon & Thurrock University Hospital , Essex , UK
Background: The techniques for the resection of renal tumors with IVC extension are based on the experience of individual units. We attempt to provide a logical approach of the surgical strategies in a stepwise fashion. Methods: Over 6-years 9 patients with renal cell carcinoma invading the IVC, underwent surgery. There were 6 males. The extension was at level IV in 4 and III in 5 cases. CPB used in 8 and hypothermia and circulatory arrest in all patients with level IV disease. The results and an algorithm of the plan of action, as per level of extension are presented. Results: Plan of action: For level I-II disease: No Cardiothoracic involvement, For level III: Cardiopulmonary Bypass (CPB) & control of the cavo-atrial junction. For level IV: use of brief periods of Circulatory Arrest & repair of the Cavotomy with a pericardial patch. Postoperative morbidity: prolonged ICU stay, 3 patients (33.3%); tracheostomy, 1 (11.1%); Sepsis, 2 (22.2%); CVA 1, (11.1%). Mortality: 2 patients (22.2%) Conclusions: Total clearance of the IVC from an adherent tumor is important, therefore extensive level IV disease presents a surgical challenge. We recommend CPB for level III and brief periods of Total Circulatory Arrest (TCA) for level IV disease.
Inferior Vena Cava (IVC) involvement in patients
undergoing surgery for renal cell carcinoma (RCC) is rare
]. The overall 5 year survival following
successful resection can be up to 40 - 50% [
], therefore one
should not preclude surgical therapy in this group of
The level of the IVC involvement as defined in the
], dictates the surgical strategies and
mandates the development of a plan of action that should be
safe, reproducible and reliable.
Favorable outcome in patients with non-metastatic
renal carcinoma and IVC involvement correlates with
complete clearance of the IVC from tumor-thrombus.
This principle sometimes can only be achieved following
an optimal exposure of the infra & supra hepatic IVC
concomitantly with clearance of the IVC -right atrial
junction. Furthermore prevention of tumor disruption
and pulmonary embolism has to be considered during
thrombectomy & manipulation of the diseased cava.
The guidelines regarding the various techniques for
the resection of RCC with IVC extension are very
scattered in the literature. In this article we attempt to
provide a systematic approach of the cardiothoracic surgical
strategies in a stepwise fashion.
Over 6-years 9 patients with RCC invading the IVC,
underwent surgery. There were 6 males. The extension
was at level IV in four(4) and III in five(5) cases. Cardio
Pulmonary Bypass was used in eight(8) patients and
hypothermia and circulatory arrest in all patients with
level IV disease. Abdominal MRI (Figure 1) is useful to
determine the extent of IVC involvement with tumor/
thrombus. Peri-operative Trans-Oesophageal Echo
(Figure 2) provides information’s regarding the amount
of adherence, supra-hepatic extension and mobility of the
tumour. Multidisciplinary approach is needed. Metastatic
disease is a contraindication for surgical therapy and has
to be ruled out. The patients characteristics are present
in appendix 1.
Mobilisation of the affected kidney with retroperitoneal
lymphadenectomy is performed first. For level I-II
disease cardiothoracic involvement is not necessary.
Limited cavotomy with the brief use of an intermittent
Caval clamp above and below the lesion is usually
adequate. The need for cardiac surgical involvement is
usually contemplated when the tumor/thrombus is
extending up to level III. We favour a standard midline
laparotomy and assessment of resectability of the renal
Following sternotomy, institution of CPB is achieved
using a split venous cannula: Superior Vena Cava &
Right femoral vein. Control of the cavo-atrial junction is
considered in order to avoid tumour embolization.
Bulky disease extending into the right atrium may be
better controlled by splitting the diaphragm through the
central tendon towards the IVC. This manoeuvre,
enables extension of the Right atrial incision towards
the IVC for direct resection of severely adhere tumours
(ie. Patient number 3).
The porta hepatis is dissected so that the liver blood
supply could be briefly interrupted (Pringle manoeuvre:
occlusion of blood inflow to the liver) during cavotomy
to further facilitate bloodless surgical field. Furthermore,
by applying a cross clamp on the sub-diaphragmatic
aorta during caval extirpation of the tumour, bloodless
operative conditions could be achieved.
Level IV involvement presents a challenge; the disease
extends into the RA with various degrees of infiltration
and adherence into the wall of IVC. Under those
circumstances the use of Total Circulatory Arrest (TCA)
has become the centre of an argument. The
pathophysiological sequelae of the use of TCA are balanced
against the risk of a suboptimal tumour clearance. We,
like others believe that with such extension of the
disease the wall of the IVC is infiltrated by tumour and
unless a complete bloodless field is instituted, only by
blunt dissections, it is impossible to achieve complete
Therefore for level IV extension of the tumour or for
suspected “suboptimal thrombectomy” for level III
disease we advocate brief period of TCA. During the
cooling period in an arrested heart the RA is opened and
tumour mobilization around the ostium of the IVC is
carried out. Endarterectomy knifes further facilitate
optimal extirpation of the tumour by negotiating anatomical
planes of excision. During TCA the cava is incised up to
10 cm cephalad in a longitudinal fashion taking care to
include with the specimen the origin of the renal vein
which is usually involved with the tumour. Clearance of
the luminal deposits of the IVC using sharp and blunt
dissections could be then carried out under direct
vision. Having mobilised the tumour proximally at the
IVC- RA junction, final extraction is usually achieved in
continuity with the nephrectomy specimen (Figure 3).
Furthermore, tumour embolization to the lungs is
avoided. This process provides a controlled bloodless
environment for facilitation of complete tumour
clearance (Figure 4). Always the cavotomy is repaired with
the use of a pericardial patch (Figure 5), in order to
avoid narrowing of the cava. An algorithm of the plan
of action, as per level of extension is depicted in
During the beginning of this program, Venovenous
bypass was used in one patient (number 7) with level III
disease. However the technique was deem cumbersome
and unsatisfactory, mainly due to excessive blood in the
surgical field, resulting in suboptimal exposure.
Cardio Pulmonary Bypass was used in eight(8) patients
and hypothermia and circulatory arrest in all patients
with level IV disease.
The operative time range from 3 hours 52 minutes to
9 hours 36 minutes. Estimated blood loss was 1850 mL
(range 950 to 3800 mL). Blood and blood product
requirement was high (7 out of nine patients). The
average blood transfusion was 2 units of red Blood Cells
(range between 1 and 4 Units). Blood products were
used in all four patients following hypothermia and
circulatory arrest. Cell-saving techniques used routinely in
Transient inotropic support by means of Dopamine
and Noradrenaline was used in 5 patients. Average
intensive care unit length of stay was 19 days (range, 1
to 164 days). In three (3) patients (33.3%) the ICU stay
was prolonged. Furthermore one (1) patient required a
tracheostomy (11.1%). Two patients developed
septicemia (one MRSA positive) and one patient develop a
CVA. Two patients died; one from septicaemia
postoperative day 55 and one from multiple organ failure
post operative day 164. The mean size of the renal mass
was 5.2 cm (range, 3.5 to 11.2 cm). Histological
examination showed renal cell carcinoma of clear type in 8
patients and papillary type in 1 patient. Lymph node
metastasis was detected in 2 patients.
Two of the discharged patients were lost to follow up.
Of the remaining five patients, 2 have had tumor
recurrence and one had pulmonary metastasis at 2 years, on
follow up chest X Ray. Those 3 patients were referred
for adjuvant chemotherapy. The cumulative
postoperative follow-up of the remaining two patients was 45
+/-11 months. They were alive at the last follow up and
free of recurrence.
Metastasis has occurred in 34.6% of the patients with
RCC and luminar propagation of the tumor into the
]. Furthermore, as per the same authors,
micrometastasis is taken place in 11.1% of those patients.
Therefore, only half of the patients with level III-IV
disease would be free of distal spread and subsequently
would benefit from an operation. Palliative resection to
control polycythemia and paraneoplastic syndromes in
patients with metastatic disease, is questionable.
Level I and II is probably the commonest entity
occurring in 60-65% of the cases and usually treated by local
resection. According to Lubahn et al [
50% of the patients with renal tumors involving the
IVC, warrant cardiothoracic involvement. Furthermore
the overall incidence of extensive IVC disease involving
the right atrium according to Bissada et al [
Hermanek et al [
] is around 27.7%.
It has been postulated that the involvement of the IVC
in RCC is generally not a vascular invasion by the
]; one could argue however, that following
removal of the thrombus-tumor from the IVC,
invariably, an area is found that indicates sub-endothelial
invasion. In addition, in 12.9% of the patients in Bissada
et al series [
] the IVC wall was invaded by tumor.
Suprahepatic extension of the tumor (level III disease)
poses a challenge, especially when the tumor is densely
adhering to the Venus wall or when the hepatic veins
contain propagating segments of tumor. Budd-Chiari
syndrome, is an extreme form of hepatic venous stasis
resulting from occlusion of the major hepatic veins or
the supra- hepatic IVC from various malignant causes,
with renal cell carcinoma being the most common. A
hepatic vein obstruction that causes Budd-Chiari
syndrome, is an adverse feature. Under such conditions,
bleeding diathesis is accelerated; this is due to Liver
congestion with reduce “synthetic function” and also
portal hypertension with the development of porta-caval
Generally for level III disease some institutions [
favor cavotomy without the use of CPB [
] or with the
use of venous-venous bypass [
]. The latter group in
a large series of patients concluded that the need for
invasive cardiovascular procedures increased the risk of
perioperative complications. The advantages of using
veno-venous bypass are restoration of hemodynamic
instability during venal clamping and the fact that there
is no need for systemic heparinization. However one
would argue that without CPB and possibly without
additional maneuvers to reduce the venus return (such
as Pringle maneuver, clamping of the abdominal aorta,
the superior mesenteric artery or the contralateral renal
artery) bloodless field cannot be achieved during
cavotomy; furthermore the imposed hemodynamic instability
at the time, has another adverse impact: the surgeon is
“pushed” to complete the extirpation of the thrombus
against the time. That can rather lead to de-bulking of
the tumor. It could also lead to dislodgment of tumor
material and subsequent pulmonary embolism.
Therefore, for level III disease, besides CPB we would
also favor the approach reported by Chowdhury et al
 whereby intermittent cross clamp of the
sub-diaphragmatic aorta is applied. This brief maneuver would
further optimize the conditions for a bloodless surgical
In the situation where the IVC is fully occluded by the
tumor in level III disease, then probably the patient may
tolerate clamping of the IVC at the junction with the
RA (under TOE guidance) without significant
hemodynamic compromise. Under those circumstances, one
could debate that CPB is not necessary. Nevertheless,
one should bear in mind the theoretical risk, that
debalking of the tumor increases the incidence of local
Five patients in our series had level III disease (Three
patients had Right side RCC). Venovenous bypass was
used in one patient. The tumor was removed
satisfactory, however hemodynamic instability and access was
deemed cumbersome. Complications with Venovenous
] and difficulty in accessing the hepatic veins
and suprahepatic cava lead us to abandoning this
For level IV disease with tumor extension in the right
atrium controversy still exists as regarding the need for
Total Circulatory Arrest (TCA). Sosa et al [
reported a poor survival for patients with level IV
disease. Cerwinka et al [
] advocates excision of
supradiaphragmatic tumors off pump with no TCA. In
contrary, Chiappini et al [
] and Mazzola et al [
claim that the use of TCA provides a safe technique for
removing the tumor thrombus in a bloodless field, and
has good early and long-term results. We, like others
] believe that when the tumor thrombus is invading
the caval wall or reaches the right atrium-ventricle then
TCA becomes a necessity. We reckon that this approach
has improved the safety and efficacy of a difficult
surgical undertaking by facilitating controlled dissection,
providing a bloodless field, and reducing the risk of tumor
embolization. The high postoperative morbidity reported
by various groups [
] is reflecting the preoperative
compromise health status of this group of patients and
possibly the use of circulatory arrest. According to
Cooper et al  the use of TCA increases up to 40%
the risk of complications and also adds up, on the
perioperative mortality. Furthermore as per Schimmer et al
] the risk of bleeding (at least theoretically) could be
exponentially higher due to: 1) profound hypothermia
itself 2) extended bypass time as a result of
coolingrewarming, and 3)the fact that those patients have
undergone extensive retroperitoneal dissections and
have accessory high pressure venous collaterals due to
the IVC obstruction.
For all those reasons aforementioned, a single
institutional approach [
] advocates in selected cases of renal
cell carcinoma with level IV IVC extension, resection of
the tumor without sternotomy, CBP, or DHCA. This
technique however has limitations ([
The need for extensive surgery with relative good
outcome has been outlined from various groups. According
to Tanaka et al [
] and Yazici and associates [
length of tumor extension is not an incremental risk
factor for adverse survival. Likewise Chiappini et al, [
states that the tumor extension into the IVC to
whatever degree is not associated with an adverse prognosis,
provided a complete resection is advocated [
Complete resection of the entire tumor is mandatory
for a reasonable attempt at a long survival, as
demonstrated by Nesbitt and colleagues [
] and Hatcher and
], where no patients with incomplete local
resection survived to 5 years. Following the same
principle we favor “Controlled Cavotomy” whereby the
interior of the IVC can be adequately inspected in a
bloodless surgical environment.
Finally, survival is also associated with the tumor
characteristics (grade of tumor cells) and lymph node
]. Throughout the literature the overall 5 year
survival is been reported to be between 40 to 50%
Five patients in our series were followed up. There
was lymph node involvement at the initial specimen of
the two patients, that had local recurrences at 2 years.
Of the remaining 3 patients, one had pulmonary
metastasis at 2 years, and 2 patients were alive at 4 years and
free of recurrence.
In summary, RCC with advance IVC involvement poses
a surgical challenge. During this report we eluded on
the pros and cons of the various approaches. In keeping
with the principles for local clearance one should
consider: multidisciplinary approach with proper
pre-operative evaluation of the extension of the tumor, optimal
control of hemodynamic conditions during cavotomy,
ability to visually assess the extent of the tumor
invasion, avoidance of tumor fragmentation and
embolization and repair of the IVC without narrowing of the
Finally in this paper, although the number of patients
reported is small, we have attempted to provide a clear
strategy for tackling a difficult and unusual entity.
Written informed consent was obtained from the
patients for publication of the series and accompanying
images. A copy of the written consent is available for
the review by the Editor-in-Chief of this journal.
Appendix 1: Patients’ characteristics.
Appendix 2: Surgical steps as per level of IVC involvement by tumor.
HP conceived of the study and wrote the manuscript with the help of MTA.
MT made valid corrections, VY organized and overlooked the progress of the
manuscript and advised on valuable points. All authors read and approved
the final manuscript.
The authors declare that they have no competing interests.
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