Gynecologic Oncology 96 (2005) 278 – 282 www.elsevier.com/locate/ygyno
Vascular anomalies in the paraaortic region diagnosed by laparoscopy in patients with gynaecologic malignancies Petra Klemma, Rosemarie Frfberb, Christhardt Kfhlera, Achim Schneiderc,* a
Department of Gynecology of the Friedrich Schiller University Jena, Germany b Institute of Anatomy I of the Friedrich Schiller University Jena, Germany c Department of Gynecology, Charite´ Universita¨tsmedizin Berlin, Germany Received 25 May 2004 Available online 11 November 2004
Abstract Objective. Paraaortic infrarenal lymphadenectomy is indicated in patients with gynecologic tumors of high metastasising potential and can be done successfully by laparoscopic approach. Vascular anomalies in this region are incidental findings during these approaches and may increase the surgical complication rate. In this study, we have documented the frequency and pattern of the vascular anomalies in paraaortic region intraoperatively and on cadavers in an attempt to increase surgical safety. Methods. A total of 86 consecutive patients underwent laparoscopic infrarenal paraaortic lymphadenectomy by a standardised technique between 1st of January 2002 and 1st of March 2004. Of the 86, 52 were primary cervical, 5 recurrent cervical, 14 endometrial, 14 early ovarian and 1 vulvar tumor with positive groin and pelvic lymph nodes. In the same time, anatomical dissections of the paraaortic region on 18 cadavers were performed at the Institute of Anatomy. Results. Arterial or venous abnormalities were identified in 30.2% (26/86) of patients by laparoscopy. The most frequent anomalies were related to atypical renal arteries (pole arteries—9 patients) and an abnormal course of lumbar veins directly draining in the left renal vein (15 patients). In one of the patients, the complete left renal vein went retroaortic to the inferior vena cava. In cadaveric dissections, vascular anomalies were noted in 44.4% (8/18) which included variations in renal and lumbar vessels and ovarian vessels. Duplicated inferior vena cava was the least common anomaly and was detected in only one case. Conclusion. During laparoscopic paraaortic inframesenteric and infrarenal lymphadenectomy, care must be taken because of possible abnormalities in arterially and venous system to avoid massive hemorrhage, transfusion and conversion to laparotomy. D 2004 Elsevier Inc. All rights reserved. Keywords: Vascular variations; Paraaortic laparoscopic lymphadenectomy; Transperitoneal approach; Abnormal renal lumbar and ovarian veins
Introduction Vascular anomalies in the paraaortic region have been well documented in the literature. Such abnormalities are due to variation in embryological development that occurs in the bilateral symmetrical precursor abdominal venous system [1–5,7,10,14,17,24]. Paraaortic lymphadenectomy is an essential part of staging and surgical therapy of gynaecological malignancies and composing the paraaortic * Corresponding author. Department of Gynecology, Friedrich Schiller University, Bachstrasse 18, 07740 Jena, Germany. Fax: +49 3641 933064. E-mail address:
[email protected] (A. Schneider). 0090-8258/$ - see front matter D 2004 Elsevier Inc. All rights reserved. doi:10.1016/j.ygyno.2004.09.056
region when treating patients with cervical, endometrial or ovarian cancer. With the introduction of laparoscopic transperitoneal and retroperitoneal lymphadenectomy in gynecologic oncology at the end of the last century, it is now feasible in part due to higher magnification to remove all the lymph nodes in the region [6,11,20,25]. In contrast to this, laparoscopic approach has to be without bleeding to reach this advantage. It is not uncommon to encounter vascular anomalies during paraaortic lymphadenectomy. For the surgeon, such anomalies are potentially hazardous and can result in vascular injury. Repair of such injury is no problem in open surgery; however, in laparoscopic transperitoneal
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lymphadenectomy, vascular complications have to be avoided since their repair is more demanding than in open surgery. Therefore, it is of utmost importance for the laparoscopic surgeon to know the frequency and pattern of venous and arterial vascular variants in the abdominal paraaortic region. This knowledge helps to avoid unnecessary hemorrhage, transfusion or conversion to laparotomy. In this study, we examined the prevalence of vascular anomalies in all patients who underwent systematic infrarenal paraaortic lymphadenectomy over a period of 2 years and compared these findings with the prevalence of abnormalities on cadavers.
Material and methods A total of 86 cancer patients underwent systematic transperitoneal laparoscopic infrarenal paraaortic lymphadenectomy at the Department of Gynecology at the University of Jena from January 2002 till February 2004 [12,19]. The procedure was indicated in patients with histologic confirmed primary endometrial cancer (n = 14), histologic confirmed primary cervical cancer (n = 52), recurrent cervical cancer (n = 5), early cancer or borderline tumor of the ovary (n = 14) or vulvar cancer with positive groin and pelvic nodes (n = 1). Complete laparoscopic infrarenal paraaortic lymphadenectomy was part of staging of gynaecologic tumors in 63 and combined with therapeutic operations in 23 patients. Staging procedure was performed in a young patient with vulvar cancer with positive pelvic nodes, in 45 patients with local advanced or nodal positive cervical cancer, in five patients with recurrent cervical cancer prior to exenteration or radiotherapy, in three patients after simple hysterectomy and bilateral salpingo-oophorectomy (BSO) for unexpected endometrial cancer, and in nine patients with unexpected early ovarian cancer. Operative treatment in addition to infrarenal paraaortic lymphadenectomy was laparoscopicassisted radical vaginal hysterectomy (LARVH) in seven patients with cervical cancer, laparoscopic assisted vaginal hysterectomy (LAVH) with BSO in 11 patients with endometrial cancer and LAVH with BSO or unilateral salpingo-oophorectomy in five patients with early ovarian cancer or borderline tumor of the ovary. All patients underwent a standardised technique for laparoscopic paraaortic lymphadenectomy by two of the authors and video recordings were taken intraoperatively (CK and AS). All the video tapes were re-examined in conjunction with an anatomist (RF) in order to evaluate the vascular anomalies. Patients details were extracted from the patient files and recorded using Excel database. In addition, in 18 cadavers which were primarily aimed for medical students education dissection of the retroperitoneal vascular anatomy with the aid of a magnifying glass was performed. All vascular variations were systematically analysed and documented by photography after marking with different colours.
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Results Complete right-sided and left infrarenal transperitoneal paraaortic lymphadenectomy was performed in all the 86 cases. The mean age for the patients group was 46.9 years (19–81) and the mean Quetelet-index 24.8 (16.2–36.9). Duration of right-sided lymphadenectomy was 31.2 min (11–87) and for left-sided infrarenal lymphadenectomy 58.5 min (15–151). On average 20.8 lymph nodes (5–52) were removed from the paraaortic region. Positive lymph nodes were found and extracted with intact capsule in 15 patients (18%). There was no major intraoperative vascular complication during the lymphadenectomy and none of the patients required blood transfusion. Similarly, there was no ureteric injury or need for conversion to laparotomy. Postoperative recovery of three patients was complicated by the development of chyloascites. One case was managed by low-fat diet, the second case required transcutaneous drainage in addition to dietary advice and the last patient underwent re-laparoscopy and drainage. In total, 30 vascular anomalies of the venous or arterial system were identified in 26 patients (30.2%). An accessory lumbar vein on the left side was encountered in 15 patients (17.4%); this accessory lumbar vein runs between aorta abdominalis and left ovarian vein up to the left renal vein (see Table 1 and Figs. 1 and 3). In addition, polar arteries, duplicated inferior vena cava, circumaortic left renal vein and retroaortic left renal vein were found (see Table 1 and Fig. 2). Two patients had three abnormalities each: a polar artery of the right and left kidney and a duplicated inferior vena cava in a patient with ovarian cancer stage Ia and a double polar artery of the right kidney, a polar artery of the left kidney and an accessory left lumbar vein in a patient with cervical cancer (see Fig. 4). All the vascular anomalies were identified intraoperatively without any complication except in two cases. In these two cases, an accessory lumbar vein draining into the left renal vein was identified following a vascular injury (blood loss less than 50 cm3) which was readily dealt with bipolar coagulation. On dissection course for student education, of the 18 cadavers 8 (44.4%) uncommon anatomical variations of the left-sided paraaortic veins were discovered (see Fig. 1). In one of the specimen, venous periaortic collar was seen. Table 1 Summary of all venous and arterial vascular abnormalities detected during laparoscopic infrarenal paraaortic lymphadenectomy Vascular abnormality
Number (n)
(1) (2) (3) (4) (5) (6)
15 7 4 2 1 1
Accessoric left lumbar vein Polar artery right kidney (1 double) Polar artery left kidney (1 double) Circumaortic left renal vein Duplicate inferior vena cava Retroaortic left renal vein
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Fig. 1. Drawings of the abnormal pattern of venous vessels in the retroperitoneal space found during 18 cadaver dissections.
After leaving the renal hilus, the left renal vein, initially a single vessel, splits into two trunks of unequal calibre which pass in front and behind the abdominal aorta to drain into a single inferior vena cava. The preaortic trunk received the left ovarian vein before passing normally into the aortomesenteric angle to reach the left side of the inferior vena
cava at the level of L1. The more voluminous retroaortic trunk received the left suprarenal vein immediately before reaching the posterior aspect of the aorta and the body of L2. In another case, the left renal vein received the left ovarian vein before passing the aorta and the lumbar column to drain into the inferior vena cava in normal position. In the third case, an uncommon left renal vein was
Fig. 2. Intraoperative atypical course of the left renal vein (1) dorsal to the aorta (2). The left ovarian vein (3), the right renal artery (4), the left renal artery (5) and the inferior mesenteric artery (6) can easily be identified.
Fig. 3. Intraoperative situs with accessory lumbar vein (1) running between aorta (2) and left ovarian vein (3) draining into the left renal vein (4). The left ureter can easily be identified (5).
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partially bifid before the trunk reunites in front of the aorta. Each trunk received one of the duplicated left ovarian veins. In four of the dissected specimen, different variants of large ascending lumbar veins with abnormal drainage into the left renal vein were found. The abnormal course of the left lumbar vein was associated in one case with an additional renal vein on the right side. A duplicated inferior vena cava of unequal calibre was found in one case. Both veins were connected one to the other by two anastomoses at the level of the left renal and the left common iliac vein. However, there were no accessory renal pole arteries seen.
Discussion Vascular anomalies of paraaortic region, such as lumbar, renal and ovarian vessel malformations, have been previously reported by many authors in various fields including radiology, anatomy and surgery. [1–5,7,8,10,11,14,16– 18,21,23,24,26,27]. Such anomalies are often incidental findings during operative procedures in the paraaortic region and are associated with an increased risk for intraoperative hemorrhage, thromboembolic events or preoperative diagnostic errors [16]. Within the venous system, the prevalence of anomalies varies between 0.1% and 43% and for the arterial system, between 9% and 31%. More rare abnormalities have been described in a number of other case reports [8,15,22]. However, the anatomic relations of the different variants of paraaortic vessels, especially of abnormal courses of left-sided lumbar veins intraoperative quite often remains obscure. Accessory renal pole arteries occur unilaterally or bilaterally as a single or a double vessel with a frequency of 9–31.3% [2–4,8,9,13,14,22,24]. In a study by Laky [14], examining 230 cadavers a unilateral supranumerary renal artery was found in 31.3% and bilateral supranumerary renal arteries in 11.7%. Since the origin of these arterial variations is not well understood, various expressions are in use for their description such as aberrant, anomalous, supernumber and lower pole artery. Bilateral accessory renal arteries can be accompanied by various abnormalities of the ovarian arteries and of the ureter [24] which may lead to hydronephrosis. Accessory lower polar arteries usually originate from the abdominal aorta. These polar arteries run ventrally over the vena cava to the right kidney and directly to the lower pole of the kidney on the left side (Fig. 4). In addition, polar arteries may originate from the common iliac artery or the median sacral artery [22]. In our study, nine (10.4%) patients who underwent paraaortic lymphadenectomy had 13 accessory polar arteries, eight arteries to the right lower pole of the kidney and five to the left lower pole. Since these accessory renal arteries are functional end arteries and do not have collaterals, inadvertent transection is not accompanied by severe hemorrhage, but leads to infarction of the lower kidney pole [8].
Fig. 4. Situs following infrarenal laparoscopic paraaortic lymphadenectomy in a patient with complex vascular abnormalities; there are two accessory renal polar arteries on the right side (1) and one on the left side (2), from which the left ovarian artery originates (3). An accessory lumbar vein on the left side (4) flows into the left renal vein. Aorta (5), vena cava (6), and inframesenteric artery (7) are labelled.
Furthermore, renal hypertension may result from a transected polar artery of the kidney [4]. The abdominal venous system develops in a very complicated way from bilateral symmetrically ordered pairs of veins that undergo partial regression and fusion on the left side leading to domination of the right side. With respect to the early embryonic development of the venous system, several variations of the renal vessels and inferior vena cava may occur. Several classification systems of the abnormalities of the vena cava and left renal vein have been published [5,10]. Transposition of the inferior vena cava was found in 0.2% to 0.55%, duplication of the inferior vena cava in 2.2% to 3.0%, a circumaortic renal collar vein in 1.5% to 8.7% and a retroaortic left renal vein in 1.8% to 2.4% [5]. Similar prevalence of the above anomalies was found in the evaluation of 1822 abdominal CT-scans and in the study of cadavers [1,7,17]. Massive hemorrhage due to retroaortic or circumaortic left-sided renal veins has been reported in the urological and vascular surgical literature [23]. Vascular injuries in 50% of patients with renal abnormalities have been described. In two patients, nephrectomy had to be performed in order to control hemorrhage and two patients died as a consequence of hemorrhage followed by thrombosis of the renal vessels [5]. In our series, we found two circumaortic renal veins (2.3%), one duplication of the vena cava (1.1%) and one complete retroaortic left renal vein (1.1%). We did not observe a transposition of the inferior vena cava. On cadaver dissection, eight (44.4%) venous abnormalities of the left renal vein and its afferent vessels were found. There are only a few studies published about typical and abnormal run of lumbar veins. With respect to the course of the lumbar veins, usually three left-sided lumbar veins are
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described in 102 open retroperitoneal lymphadenectomies; in 43% of patients, an atypical course of one lumbar vein draining into the left-sided renal vein was identified [3]. In our series, an atypical course of a left-sided lumbar vein was observed in 15 (17.4%) patients who had underwent laparoscopic lymphadenectomy and in four dissected cadavers (22.2%). Pelvic and paraaortic lymphadenectomy are an integral part of staging and surgical treatment of patients with gynecologic malignancies. Benedetti-Panici et al. [4] reported vascular abnormalities in 13.6% of 309 patients who underwent open lymphadenectomy for the treatment of cervical, endometrial or ovarian cancer. In 3 (1%) out of these 309 patients abnormalities were diagnosed following a hemorrhagic event. In our series, the prevalence of venous and arterial abnormalities was higher at 30% which is probably due to the more accurate laparoscopic dissection which results from a less bloody field with 7 magnification. An awareness of the existence of possible venous or arterial anomalies within the abdominal retroperitoneum is an essential prerequisite for laparoscopic paraaortic lymphadenectomy in order to avoid hemorrhage, transfusion and conversion to laparotomy.
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