Assessment of para-aortic lymph nodes by intraoperative sonography in gynecological malignancies: a preliminary report

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Ultrasound Obstet Gynecol 2003; 22: 622–626 Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.928

Assessment of para-aortic lymph nodes by intraoperative sonography in gynecological malignancies: a preliminary report E. RYO*, T. NAGASAKA*, T. YASUGI†, S. KOZUMA† and Y. TAKETANI† *Musashino Red Cross Hospital and †Department of Obstetrics and Gynecology, University of Tokyo, Tokyo, Japan

K E Y W O R D S: cervical carcinoma; endometrial carcinoma; gynecological malignancies; intraoperative sonography; ovarian carcinoma; para-aortic lymph nodes

ABSTRACT

INTRODUCTION

Objective To investigate the usefulness of intraoperative sonography for the assessment of para-aortic lymph nodes in gynecological malignancies.

The assessment of para-aortic lymph nodes is very important in determining the spread of gynecological malignancies. Various procedures have been used to assess them, i.e. image diagnosis such as computed tomography (CT), palpation during surgery, biopsy of enlarged nodes, and systemic para-aortic lymphadenectomy. It is obvious that systematic lymphadenectomy is the most accurate of these methods to detect lymph node metastasis. However, it is not regarded as a standard procedure due to its increased operation time and surgical morbidity. Currently, the prevailing notion is that swollen lymph nodes must be palpated and biopsied. However, intraoperative assessment by palpation is frequently incorrect1,2 , as is image assessment of para-aortic nodes by CT3 – 6 . Many metastatic para-aortic nodes are too small to be detected by these methods. High-resolution transabdominal sonography can theoretically detect such small regions. However, it overlooks metastatic nodes as frequently as does CT4,7 . The main reason for this is that ultrasound is attenuated and scattered by the abdominal wall and bowel. In contrast, intraoperative sonography makes it possible to scan the para-aortic regions directly. The purpose of this study was to investigate the usefulness of intraoperative sonography in assessing para-aortic lymph nodes in gynecological malignancies.

Methods The assessment of para-aortic lymph node swelling by computed tomography (CT), palpation during surgery and intraoperative sonography was performed in 43 women with a gynecological malignancy. The sensitivity, specificity and predictive values of each technique for assessment of node metastasis were examined in the 33 women who underwent para-aortic lymphadenectomy. For each of the three assessment techniques, the number of para-aortic lymphadenectomies that would have been performed and the number of women who would have had missed metastasis were evaluated assuming a paraaortic lymphadenectomy would be performed only when swollen nodes were detected. Results Para-aortic nodes were assessed to be swollen by CT, palpation, and intraoperative sonography, respectively, in one, six and 10 of 43 women in total, and in one, six and nine of the 33 women who underwent para-aortic lymphadenectomy. The sensitivity and negative predictive value of intraoperative sonography were 100%, while the specificity and positive predictive value of CT were 100%. If para-aortic lymphadenectomy had been performed only when swollen nodes were detected by intraoperative sonography, the number performed would have decreased from 33 to nine without missing lymph-node metastasis. Conclusion Intraoperative sonography has potential for the assessment of para-aortic lymph nodes in gynecological malignancies. Copyright  2003 ISUOG. Published by John Wiley & Sons, Ltd.

METHODS A total of 43 women with a gynecological malignancy who underwent surgery at our hospital were recruited for this study. There were 24 cases of endometrial carcinoma, seven cases of ovarian carcinoma, 11 cases of cervical

Correspondence to: Dr E. Ryo, Department of Obstetrics and Gynecology, Teikyo University, School of Medicine, 2-11-1, Kaga, Itabashi-ku, Tokyo, 173-8606, Japan (e-mail: [email protected]) Accepted: 8 August 2003

Copyright  2003 ISUOG. Published by John Wiley & Sons, Ltd.

ORIGINAL PAPER

Intraoperative sonography of aortic lymph nodes

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Table 1 Number of patients and clinical stages for each gynecological malignancy (n = 43)

Table 2 Results of para-aortic lymphadenectomy Site of disease

Site of disease

FIGO stage

Cervix Ia Ib IIb IIIb

11 1 3 5 2

Ib Ic IIa IIb IIIa IIIb IIIc IVb

24 10 5 2 2 1 1 1 2

Ic IIIb IIIc

7 2 1 4

I

1 1

Endometrium

Ovary

Sarcoma Total

Patients (n)

PAN metastasis

Cervix Endometrium Ovary Uterus (sarcoma)

4 21 7 1

1 2 3 0

Total

33

6

Patients (n)

43

carcinoma, and a case of uterine leiomyosarcoma. Table 1 shows the clinical staging and the number of women with each gynecological malignancy. Neither chemotherapy nor radiation therapy was performed before surgery except in two patients who had stage IIIb cervical carcinoma and received neoadjuvant chemotherapy. All women gave informed consent, and the study was approved by the hospital ethics committee. As a general rule, in cases of endometrial and ovarian carcinoma and the one case of uterine leiomyosarcoma, hysterectomy in association with salpingo-oophorectomy, omental biopsy, and pelvic and para-aortic lymphadenectomy were performed because these procedures have been reported to improve the survival of these patients8,9 . In cases of cervical carcinoma, hysterectomy, with or without salpingo-oophorectomy, and pelvic but not paraaortic lymphadenectomy were performed. However, for clinical reasons (which did not include the results of the para-aortic node assessment) para-aortic lymphadenectomy was not performed in three cases of endometrial carcinoma, and it was performed in four cases of cervical carcinoma. Consequently, a total of 33 women underwent para-aortic lymphadenectomy. Para-aortic lymph node metastasis was found in six of these women (Table 2) and the average number of para-aortic nodes removed per woman was 18. Before surgery, CT was performed with a helical scanner (Hispeed NX, Lightspeed Plus, GE and Yokogawa medical system, Tokyo, Japan) at the level between the aortic bifurcation and the renal vessels, and transverse images 5 mm in thickness were obtained at 9-mm intervals. The window level and window width were 80–100 and 300–350 Hounsfield Units, respectively. All women received 2 mL/kg non-ionic

Copyright  2003 ISUOG. Published by John Wiley & Sons, Ltd.

PAN, para-aortic lymph node.

intravenously administered contrast medium (Optiray 320; Yamonouchi, Tokyo, Japan) at a rate of 2–2.5 mL/s. A structure adjacent to the aorta or the vena cava was identified as a swollen node if it had a well-defined round shape with soft-tissue attenuation, its diameter was more than 5 mm, and it could not be enhanced to the same degree as adjacent blood vessels. In addition, if more than one of the structures was present, they were identified as swollen nodes even if they were less than 5 mm in diameter. These assessments were performed by at least two radiologists, each with more than 10 years’ experience. The procedures during surgery were as follows. The woman was placed in the lithotomy position under general anesthesia, and the lower abdomen was opened via a midline incision. After laparotomy, an operator, blinded to the results of CT, palpated the para-aortic region and assessed whether the para-aortic lymph nodes were swollen. Next, an examiner, blinded to the results of CT and palpation, inserted an ultrasound probe into the upper abdomen. By making contact with the retroperitoneum, the examiner scanned the para-aortic region at the level between the aortic bifurcation and the renal vessels, and assessed for swollen nodes. First, the left latero-aortic area was scanned by moving the ultrasound probe from the aortic bifurcation to the origin of the renal vessels. Both the bifurcation and the renal vessels could be observed by ultrasonography. Then the preaortic and retro-aortic areas, inter-aorticocaval area, pre-caval and retrocaval areas, and right latero-caval area were scanned in the same way. If a hypoechoic welldefined apparently round structure was found, its shape was confirmed to be round by further observations from more than two different directions to exclude vessels. A hypoechoic well-defined round structure adjacent to the aorta or the vena cava was identified as a lymph node, and it was assessed to be swollen if its diameter was more than 5 mm. If more than one of the structures was present, they were identified as swollen nodes even if they were less than 5 mm in diameter. The operators were gynecologists with more than 10 years’ experience and the examiner was an ultrasound specialist. The ultrasound machine was an Aloka SSD-2000 system (Aloka, Tokyo, Japan) with a UST-995 7.5-MHz probe (Figure 1). In those patients who underwent para-aortic lymphadenectomy, an abdominal incision was extended to the subxyphoidal region after hysterectomy with pelvic

Ultrasound Obstet Gynecol 2003; 22: 622–626.

Ryo et al.

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Figure 1 Photograph of a UST-995 7.5-MHz probe.

lymphadenectomy. The procedure involved complete dissection of the lymph nodes from the aortic bifurcation up to the renal vessels. To achieve this, we mobilized the ascending colon, the descending colon and the duodenum, and displaced them to the right, to the left and upwards, respectively, so that the para-aortic retroperitoneal space was widened up to the renal vessels. Lymphatic tissue surrounding the retroperitoneal vessels was removed completely. The removed lymphatic tissue was examined to confirm whether swollen lymph nodes detected by CT, palpation, and intraoperative sonography were actually lymph nodes. Lymph node metastasis was examined microscopically by the hospital pathologists. Thus, swollen lymph nodes were assessed by CT, palpation during surgery, and intraoperative sonography in all 43 women. These assessments were then confirmed by macroscopic observation of removed lymphatic tissue in the 33 women who underwent para-aortic lymphadenectomy, and the sensitivity, specificity, and positive and negative predictive values of the individual techniques for assessment for lymph node metastasis were calculated. We also considered for each of the three assessment techniques what the clinical consequences would have been if paraaortic lymphadenectomy had been performed only when swollen lymph nodes were detected, in terms of the number of para-aortic lymphadenectomies performed, and the number of women who would not have undergone lymphadenectomy in spite of having node metastasis (i.e. the number of women with missed metastasis).

by examination of the removed lymphatic tissue, with the exception of one woman whose lymph nodes were assessed to be swollen by palpation but proved to have atherosclerosis of the aorta. Therefore, CT, palpation, and intraoperative sonography detected swollen lymph nodes accurately in one, 5, and 9 of the 33 women, respectively. There were no swollen nodes larger than 5 mm that could not be detected by intraoperative sonography. Assessments of swollen nodes, therefore, almost completely coincided with the examination of removed lymphatic tissues. Figure 2 shows an example of swollen para-aortic lymph nodes detected by intraoperative sonography in a woman with endometrial carcinoma. Their cross-sectional diameters were less than 1 cm. Neither CT nor palpation could detect the nodes in this case. The lymph nodes proved to be metastasized. Para-aortic lymph node metastasis was present in six women. Table 3 shows the sensitivity, specificity, and positive and negative predictive values of the individual assessments for lymph node metastasis. All women with metastasis had swollen nodes detected by intraoperative sonography. Therefore, both sensitivity and negative predictive value were 100% by this method, while specificity and positive predictive value of CT were 100%. Table 4 shows for each of the three assessment techniques the number of para-aortic lymphadenectomies that would have been performed (i.e. the number with swollen lymph nodes detected) and the number of women who would have had missed metastasis (i.e. false negatives) assuming a para-aortic lymphadenectomy was performed only when swollen nodes were detected.

Lymph node Aorta

Vena cava Vertebra

Lymph node

RESULTS Of the 43 women recruited for the study, swollen paraaortic lymph nodes were detected in one, six, and 10 by CT, palpation, and intraoperative sonography, respectively. Both palpation and sonography took around 1 min and had no adverse effects in all cases. Of the 33 patients who underwent para-aortic lymphadenectomy, lymph nodes were assessed to be swollen in one, 6, and 9 by CT, palpation and intraoperative sonography, respectively. All were confirmed to be lymph nodes

Copyright  2003 ISUOG. Published by John Wiley & Sons, Ltd.

Aorta

Figure 2 Intraoperative cross-sectional (a) and longitudinal (b) ultrasound images showing swollen para-aortic lymph nodes with metastasis. Neither computed tomography nor palpation could detect the lymph nodes.

Ultrasound Obstet Gynecol 2003; 22: 622–626.

Intraoperative sonography of aortic lymph nodes

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Table 3 Sensitivity, specificity and positive (PPV) and negative (NPV) predictive values of three assessment techniques for para-aortic lymph node metastasis

Method

Sensitivity (% (n))

Specificity (% (n))

PPV (% (n))

NPV (% (n))

Computed tomography Palpation Intraoperative sonography

16.7 (1/6) 66.7 (4/6) 100 (6/6)

100 (27/27) 92.6 (25/27) 88.9 (24/27)

100 (1/1) 66.7 (4/6) 66.7 (6/9)

84.4 (27/32) 92.6 (25/27) 100 (24/24)

Table 4 Number of para-aortic lymphadenectomies that would have been performed and number of women who would have had missed metastasis if para-aortic lymphadenectomy (PALA) had been performed only when swollen lymph nodes were detected by each of three assessment techniques, along with the numbers in reality

Method Theoretical Computed tomography Palpation Intraoperative sonography Actual Routine PALA

Performed PALA (n)

Missed metastasis (n)

1 6 9

5 2 0

33

0

The number of actual procedures of routine para-aortic lymphadenectomy is also shown for comparison.

DISCUSSION For proper staging of gynecological malignancies, thorough exploration of the retroperitoneal space is mandatory to detect metastasis of pelvic and para-aortic lymph nodes. It would be useful in planning surgery to be able to predict the likelihood of retroperitoneal lymph node positivity preoperatively. At present, methods used for the assessment of lymph nodes are diverse and ineffective. However, data on how accurately these methods predict lymph node positivity are scant. We found that CT, widely employed for the assessment of para-aortic lymph nodes, failed to detect most metastatic nodes, with a sensitivity of 16.7%. Blythe et al.10 stated that para-aortic lymph node biopsies should be included in the routine evaluation of patients with gynecological malignancies. Onda et al.11 stated that aortic lymph nodes above the inferior mesenteric artery and the internal and external iliac and obturator lymph nodes are essential sites for lymph node biopsy in ovarian carcinoma. However, the appropriate method of biopsy for assessing lymph node involvement in gynecological malignancies has yet to be determined. Currently, a widely preferred notion is that swollen paraaortic lymph nodes must be palpated and biopsied during surgery if necessary. However, assessment by palpation fails to detect metastatic nodes in many cases; we found that metastasis was missed by palpation in two of six (33.3%) women. It goes without saying that routine lymphadenectomy is the most accurate method for assessing lymph node

Copyright  2003 ISUOG. Published by John Wiley & Sons, Ltd.

metastasis. In hindsight, however, most of our patients (27/33; 81.8%) had no node metastasis and suffered unnecessary morbidity. An accurate method of predicting the node positivity would be of great value. Unfortunately, in principle, it is not possible to avoid both missed metastasis and unnecessary surgical morbidity; high sensitivity and negative predictive value are especially indispensable, considering the serious consequences of missed metastasis. We found intraoperative sonography to have 100% sensitivity and negative predictive value and it thus may enable us to avoid unnecessary lymphadenectomy. If we had performed para-aortic lymphadenectomy only when swollen lymph nodes were detected using sonography in this series of clinical investigations, we could have reduced the number of para-aortic lymphadenectomies from 33 to nine without missing any metastasis. We believe that most gynecologists are convinced of the superiority of transvaginal sonography to the transabdominal approach, CT scanning, and magnetic resonance imaging in the observation of the contents of the pelvis near the vagina. The proximity at which the transvaginal probe can be placed to the contents of the pelvis, in combination with the higher transducer frequencies used, results in vastly superior resolution. In the same way, the intraoperative approach with higher sonic frequencies was able to demonstrate a clear image of the aortic regions and lymph nodes. There were nine women who had no swollen nodes detected by intraoperative sonography and who did not undergo para-aortic lymphadenectomy, and seven of these received neither chemotherapy nor radiation therapy to the para-aortic regions. At the time of writing, these seven women had been cancer-free for a period of more than 2 years and 7 months since surgery. Including these seven in the calculation of the negative predictive value for lymph node metastasis makes no difference to the value (31/31, 100%). Though this study was preliminary and the patient number was small, the results are encouraging and warrant further investigation. It appears that intraoperative sonography has potential for assessing para-aortic lymph nodes in gynecological malignancies.

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