Comparative analysis of the results of surgical treatment of kidney cancer complicated by tumor thrombosis of renal vein and inferior vena cava of level I–II

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Introduction

Renal cell carcinoma (RCC) accounts for about 3% of cases in the statistics of all oncourological diseases. In terms of prevalence, this type of oncopathology is in third place, second only to prostate and bladder cancer. Nevertheless, in terms of mortality, renal cell carcinoma confidently holds first place [1].

As of 2022, over 420 thousand new cases of RCC have been diagnosed worldwide. In Russia, RCC in the population accounts for 4.8 % among men and 3.4 % among women in the structure of malignant neoplasms. In 2018, about 14 thousand new cases of cancer were registered, and the standardized incidence rate reached 17 cases per 100 thousand population. Thus, the total increase over a ten-year period was almost 25 %¹.

Moreover, venous thrombosis of tumor origin occurs in up to 14 % of cases in patients with renal cell carcinoma, and the possibility of its spreading to the right parts of the heart remains in approximately 1 % of cases [2].

Surgical tactics are determined by the cranial border of the thrombus [3]. Therefore, clinical staging of kidney cancer with tumor thrombosis is of particular relevance. Several surgical classifications of tumor thrombus levels are proposed. The most common remains the Mayo classification of 2004, according to which tumor thrombus of the renal vein is divided into the following levels [4]:

• level 0 – the thrombus is limited to the borders of the renal vein;
• level I – the tumor thrombus is located at a distance of less than 2 cm from the orifice of the renal vein;
• level II – the tumor thrombus extends to the IVC more than 2 cm above the renal vein, but below the hepatic veins;
• level III – the tumor thrombus extends above the hepatic veins, but below the diaphragm;
• level IV – the tumor thrombus is located above the level of the diaphragm.

Patients diagnosed with renal cell carcinoma (RCC) and the presence of a tumor thrombus in the inferior vena cava have an unfavorable prognosis, but early diagnosis and surgical treatment significantly increase the chances of a successful prognosis. To date, open-access surgery remains one of the most effective methods for treating patients with RCC against the background of tumor thrombosis of the renal and inferior vena cava of levels 1–2 [5]. Recently, the laparoscopic method has been successfully used, which has certain advantages over the classical (laparotomic) technique of surgical intervention [6]. At the Russian Scientific Center of Radiology and Surgery named after Academician A.M. Granov, both types of access were used from 2007 to 2024, depending on the indications and somatic status of the patient.

The following criteria are used to make a diagnosis:

• visualization of neoplasm and tumor thrombus in the lumen of the renal and inferior vena cava according to ultrasound data;
• determination of kidney neoplasm accumulating contrast agent and tumor invasion into the renal and inferior vena cava using CT, MRI;
• morphological verification based on biopsy or surgical material, if necessary.

It should be noted that surgical interventions in patients with tumor thrombosis are difficult to implement technically. In addition, RCC has pronounced hypervascularization, which increases the risk of profuse bleeding during surgery for large tumors.

As a result of the operation in patients with locally advanced RCC, radical nephrectomy with thrombectomy makes it possible to ensure a two-year overall survival rate of up to 96.9 % [7]. However, without the thrombectomy stage, the prognosis remains extremely unfavorable.

Although traditional (laparotomic) nephrectomy is considered a traditional approach, it has significant disadvantages – severe surgical trauma, extensive blood loss and a long rehabilitation period [8; 9].

Materials and Methods

100 patients diagnosed with kidney cancer complicated by tumor venous thrombosis of the renal and inferior vena cava levels 1–2 were studied at the Russian Research Center for Radiology and Surgical Technologies named after Academician A.M. Granov in the period 2007–2024. There were 54 men and 46 women. The average age of patients was 56 (24–85) years (Fig. 1). 50 patients underwent open surgery, 50 patients underwent laparoscopic surgery. In the laparoscopy group, 8 patients underwent conversion of the access as a result of: tumor thrombus invasion into the wall of the inferior vena cava, peritoneal commissures, uncontrolled bleeding.

 

Fig. 1. Age of patients, years

 

Clinical manifestations of renal cell carcinoma with thrombosis were detected in 35 (35 %) of patients. The most common symptoms were:

• lumbar pain – in 11 patients (11 %);
• prolonged fever of unknown genesis – in 7 (7 %);
• weight loss of 10 kg in less than six months – in 7 (7 %);
• macrohematuria – in 10 (10 %).

All patients had a kidney tumor – 38 (left), 62 (right). Category T was assessed in all patients. Stage pT3a was established in 54 (54 %) patients, pT3b – in 46 (46 %). Tumor venous thrombus was observed in 100 % of patients. It was determined in 54 people in the renal vein; invasion to the inferior vena cava was no more than 2 cm – in 28 (1st level of thrombus according to Mayo) and more than 2 cm to the mouth of the hepatic veins in 18 (2nd level of thrombus according to the Mayo) (Fig. 2).

 

Fig. 2. Thrombus level in patients, %

 

All patients underwent the following at the pre-hospital stage: ultrasound of the kidneys, CT of the abdominal and retroperitoneum spaces with intravenous contrast. If necessary, patients also underwent MRI venography at the pre-hospital stage. In some patients, the results of MRI with venography revealed signs of invasion into the vessel wall – the renal vein (RV) or IVC. Such patients underwent cavography at the preoperative stage for additional assessment of the presence of invasiveness to the vascular wall. Those patients who, according to MRI data, had extensive invasion into the wall of the IVC, underwent classical surgery with resection and prosthetics of the inferior vena cava segment.

The second level thrombus was observed in 18 patients (18 %), 2 of them had a complete block of the IVC from the point of entry of the renal vein to the subhepatic region (they underwent open surgery), 3 had a partial block, 60 % had occlusion, the vascular occlusion in most patients with the 2nd level of tumor thrombus was no more than 35–40 %.

Some patients underwent preoperative renal embolization to reduce/stop hematuria and reduce the extent of the tumor thrombus. During embolization, a contrast agent was injected into the vessels to ensure sufficient visualization of the vascular architecture of the affected kidney. The localization of the vascular branches through which blood enters the affected kidney was determined. Then, the emboli that caused the blockage were introduced through the catheter. The beginning of the surgical stage was the mobilization of the ascending / descending colon, the duodenum, then the exit to the aorta and the inferior vena cava.

There were differences in kidney mobilization: the right kidney was mobilized after renal artery ligation/clipping, but before tumor thrombus removal; the left kidney was mobilized after renal artery clipping and thrombectomy from the IVC.

The technique for performing thrombectomy was selected based on the length, diameter of the tumor thrombus, its spread in the inferior vena cava, as well as the extent of tumor invasion into the vessel wall.

Depending on the location of the thrombus in the IVC, the affected area was isolated: vascular “bulldog” clamps were applied above and below the thrombus. Then the clamp was applied to the contralateral renal vein. At the next step dissection of the the wall of the inferior vena cava was made to extract the tumor thrombus. After thrombectomy, the defect in the wall of the inferior vena cava was sutured with a continuous suture. Almost all patients underwent lymph node dissection.

All patients were prescribed fractionated heparin in the early postoperative period, and then they were transferred to anticoagulant treatment under the supervision of a cardiologist. As recovery progressed, anticoagulant therapy was discontinued and antiplatelet drugs were prescribed as a continuous treatment.

Technique of operation. The classical method was used to access the affected kidney laparoscopically, with the patient positioned on the healthy side. In case of damage to the left kidney with a tumor thrombus of the 1st level, access was carried out through the left lateral canal. In case of a tumor thrombus of the 2nd level, repositioning to the opposite side was performed for further manipulations. Mobilization and retraction of the medial part of the colon was performed after installing an additional port along the midline of the abdomen and in the hypochondrium along the parasternal line.

In order to perform aortocaval and paracaval lymph node dissection, visualization of the common iliac vein was performed with subsequent transition to the IVC. At this stage, mobilization of both the IVC and the contralateral renal vein was performed. The renal artery was then isolated, clipping it three times with Hem-o-lock clips. After the clipped renal artery was crossed, the renal vein was isolated, a tumor thrombus was identified in its lumen. A tourniquet or a vascular "bulldog" clamp was applied to the distal and proximal edge of the mobilized inferior vena cava and the contralateral renal vein. The lymph node dissection stage was performed after dissection of the anterior wall of the IVC, extraction of the thrombus from its lumen and suturing of the wall of the inferior vena cava. Fig. 3–9 show data for tumor thrombus levels 1–2.

A feature of thrombectomy for thrombi corresponding to the 1st level according to Mayo: in case of tumor thrombosis of the 1st level, a Satinsky clamp was applied through an additional port on the IVC above the renal vessels, which made it possible to push back the top of the thrombus. In addition, vascular tourniquets and bulldog clamps were used to isolate the IVC segments. Laparoscopic scissors were used to dissect the wall of the inferior vena cava and extract the thrombus. The wall defect was sutured with a continuous suture. After that, the Satinsky clamp, vascular clamps from the distal, proximal parts of the IVC and the contralateral renal vein were removed step by step. The specimen was removed through an extended incision in the iliac region.

Features of thrombectomy for thrombi corresponding to Mayo level 2: four trocars were installed, as in standard nephrectomies. One port was used for the camera, two working and an additional one for liver retraction. Clipping and transection of the gonadal and lumbar veins were performed in the course of the IVC mobilization (1–2). Vascular tourniquets / bulldogs were placed under the IVC and put above and below the borders of the tumor thrombus. An additional tourniquet was placed under the left renal vein.

 

Fig. 3. Visualization before surgery: the tumor thrombus is located in the left renal vein to the inferior vena cava: a – 2 cm – the thrombus corresponds to the 1st level according to Mayo; b – the thrombus corresponds to the 2nd level according to the Mayo

 

Fig. 4. Stage of application of vascular tourniquets to the inferior vena cava below and above the cranial border of the tumor thrombus, dissection of the wall of the renal vein at the site of entry into the inferior vena cava

 

Fig. 5. Stage of dissection of the wall of the left renal vein with “dislocation” of the tumor thrombus from the lumen of the vessel. The apex of the tumor thrombus (yellow)

 

Fig. 6. Application of a metal clip to the renal vein stump

 

Fig. 7. Stage of single-step dissection and clipping of the right renal vein with the displaced tumor thrombus from the inferior vena cava into the lumen of the renal vein

 

Fig. 8. Stage of extraction of tumor thrombus from the inferior vena cava

 

Fig. 9. Stage of suturing the wall of the inferior vena cava after extraction of the tumor thrombus (restoration of the integrity of the vascular wall)

 

Results and Discussion

The median operating time in patients operated on using laparoscopic access was 127.5 min, the volume of blood loss was 200 ml; in the laparotomy group – 132.5 min, the volume of blood loss was 250 ml in the course of surgical intervention. Complications were found in 8 patients (8 %) (Fig. 10).

 

Fig. 10. Intraoperative data of laparoscopy and laparotomy

 

Early complications according to the Clavien – Dindo classification (first, second and third class) were observed in 33 patients (33 %): of the first class according to the Clavien-Dindo classification – in 20 patients (20 %), the second class (pneumonia, intestinal paresis) – in 8 (7 %), third class (subcutaneous hematoma, abscess, seroma) – in the third class – 3 (3 %), and the fourth class – in 2 (2 %). Complications were of various nature, including posthemorrhagic anemia, electrolyte abnormalities according to laboratory data, changes in the functions of internal organs, pneumonia, intestinal paresis, abscess and hematomas of the postoperative wound, thromboembolia of the pulmonary artery. In patients operated by open access, the list of early complications included: prolonged pain syndrome, dynamic intestinal obstruction, lower lobe pneumonia, hematomas and abscess in the area of the postoperative wound. Recovery occurred on the 4th–5th postoperative day with the administration of drugs to activate intestinal motility, when the rates of early postoperative complications were lower in the group of patients operated by laparoscopic access (Fig. 11, а).

 

Fig. 11. Postoperative complications: a – early; b – late

 

Late postoperative complications were observed in 4 patients (anterior abdominal wall hernia, peritoneal commissures), of which 3 were from the group operated on via laparotomy access, and one was from the laparoscopy group, who underwent conversion of the access due to extensive invasion of the tumor thrombus (Fig. 11, b).

Histological examination showed renal cell carcinoma in all cases.

84 cases (84 %) – clear cell carcinoma, 9 (9 %) – papillary carcinoma, 4 (4 %) – chromophobe, 2 (2 %) – medullary, one case (1 %) – clear cell-papillary. The degree of anaplasia according to Fuhrman G1–2 was observed in 65 cases (65 %), G3 – in 24 (24 %), G4 – in 11 (11 %). The thrombus had a typical structure, which repeated the structure of the tumor in the kidney (Fig. 12).

 

Fig. 12. Features of histological examination of the tumor

 

Patients stayed in hospital for 6 to 13 days after laparoscopic intervention, with open surgery – from 7 to 18. The need for analgesics in patients after laparotomy access was from 2 to 5 days, laparoscopy – from 1 to 3 days (Fig. 13).

 

Fig. 13. Days of hospitalization and prescription of analgesics

 

Despite the fact that modern medicine is actively advancing in the treatment of RCC, the only effective method that gives hope for a recovery remains nephrectomy with thrombectomy from the inferior vena cava.

The main difficulty of thrombectomy for IVC thrombosis of levels 1–2 is control of the upper border of the thrombus, which is located in an area that is difficult to access according to anatomical indicators. According to our data, the choice of thrombectomy technique for thrombosis of levels 1–2 is individual (Fig. 14).

 

Fig. 14. Result of laparoscopic nephrectomy with thrombectomy from the inferior vena cava (kidney tumor size 12.4×11.3×7.6 cm)

 

Despite the fact that surgical treatment of kidney cancer is associated with technical difficulties, as well as a difficult postoperative period, classical nephrectomy with thrombectomy provides a 5-year overall survival rate of up to 70 % [10; 11].

Patients without metastatic lesions have a chance of a positive outcome with radical surgery.

In patients with oligometastatic renal cell carcinoma, cytoreductive nephrectomy improves the conditions for systemic therapy and increases overall survival [12].

Since the tumor has extremely unfavorable morphological characteristics, the frequency of disease progression is quite high and is at least 38%. In this regard, radical intervention and removal of the pathological kidney remains the only effective method of treating this category of patients [13] (Fig. 15).

 

Fig. 15. Surgical approach for open nephrectomy with thrombectomy from the IVC. Stage of layer-by-layer suturing of the tissues of the anterior abdominal wall

 

Conclusions

Thus, based on the conducted study, we conclude that classical nephrectomy with thrombectomy remains an effective method of treating patients with renal cell carcinoma with invasive tumor venous thrombosis of 1–2 levels.

The negative side of laparotomy access is greater surgical trauma, the need for long-term administration of analgesics, the number of early and late postoperative complications and a longer period of patient rehabilitation. According to intraoperative and postoperative indicators, laparoscopic access is less traumatic. Conventional laparotomic nephrectomy with thrombectomy is the gold standard for the treatment of locally advanced renal cell carcinoma at stage pT3a and pT3b, but laparoscopic approach is an effective alternative. The above study clearly demonstrates this.

 

¹ Global Cancer Observatory 2022 [electronic resource], available at: https://gco.iarc.fr/today/en/dataviz/ pie?mode=population&group_populations=0&cancers=29

About the authors

M. K. Mirzabekov

Russian Research Center for Radiology and Surgical Technologies named after Academician A.M. Granov

Author for correspondence.
Email: Musabek.mirzabekoff@yandex.ru
ORCID iD: 0009-0003-8365-7672
SPIN-code: 5892-4003

Postgraduate of the Department of Radiology, Surgery and Oncology

Russian Federation, Saint Petersburg

M. I. Shkolnik

Russian Research Center for Radiology and Surgical Technologies named after Academician A.M. Granov

Email: Musabek.mirzabekoff@yandex.ru
ORCID iD: 0000-0003-0589-7999
SPIN-code: 4743-9236

PhD (Medicine), Associate Professor of the Department of Radiology, Surgery and Oncology, Senior Researcher

Russian Federation, Saint Petersburg

O. A. Bogomolov

Russian Research Center for Radiology and Surgical Technologies named after Academician A.M. Granov

Email: Musabek.mirzabekoff@yandex.ru
ORCID iD: 0000-0002-5860-9076
SPIN-code: 6554-4775

DSc (Medicine), Associate Professor, Professor of the Department of Radiology, Surgery and Oncology, Chief Researcher

Russian Federation, Saint Petersburg

D. G. Prokhorov

Russian Research Center for Radiology and Surgical Technologies named after Academician A.M. Granov

Email: Musabek.mirzabekoff@yandex.ru
ORCID iD: 0000-0001-5795-337X
SPIN-code: 5957-6715

PhD (Medicine), Senior Researcher

Russian Federation, Saint Petersburg

References

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