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Ultrasound Obstet Gynecol 2008; 32: 91–96

Published online in Wiley InterScience (www.interscience.wiley.com). DOI: 10.1002/uog.5366

Diagnostic value of intraoperative ultrasonography to assess


para-aortic lymph nodes in women with ovarian and uterine
corpus malignancy
E. RYO
Department of Obstetrics and Gynecology, Teikyo University, Tokyo, Japan

K E Y W O R D S: endometrial carcinoma; intraoperative ultrasonography; ovarian carcinoma; para-aortic lymphadenectomy;


para-aortic lymph node

ABSTRACT metastasis. Its high negative predictive value allows


avoidance of unnecessary para-aortic lymphadenectomy
Objectives To examine the ability of intraoperative
in women with ovarian and uterine corpus malignancy.
ultrasonography to detect enlarged para-aortic lymph
Copyright  2008 ISUOG. Published by John Wiley &
nodes, and to assess its potential use in reducing the
Sons, Ltd.
number of unnecessary para-aortic lymphadenectomies
performed in women with ovarian and uterine corpus
malignancies.
INTRODUCTION
Methods Computed tomography (CT), palpation during
surgery, and intraoperative ultrasonography were used to Para-aortic lymph nodes are regional lymph nodes of
assess whether para-aortic lymph nodes were enlarged in ovarian and endometrial carcinomas, and determining
163 women with ovarian and uterine corpus malignancy. whether or not they are metastasized is very important
All the women underwent para-aortic lymphadenectomy, in assessing spread of the cancer. Up to now, there has
and nodes were assessed for metastasis. been no reliable procedure other than systematic para-
aortic lymphadenectomy for assessment; however, routine
Results Thirty-five women had pathological para-aortic
lymphadenectomy increases surgical morbidity and its
node metastasis. The sensitivity, specificity, and positive
therapeutic significance is uncertain.
and negative predictive values of CT for the diagnosis
In a preliminary report1 it was suggested that
of metastasis were 42.9, 96.1, 75.0 and 86.0%,
intraoperative ultrasonography has a superior negative
respectively. These values were 60.0, 82.0, 47.7 and
predictive value (NPV) and sensitivity to preoperative
88.2% for palpation, and 91.4, 69.5, 45.1 and 96.7%
computed tomography (CT) and palpation during surgery
for intraoperative ultrasonography, respectively. If para-
in detecting para-aortic node metastasis in gynecological
aortic lymphadenectomy had been performed only when
malignancies. The purpose of this study was to further
enlarged lymph nodes were detected on CT then the
assess the ability of intraoperative ultrasonography to
number performed would have been reduced from 163
detect enlarged para-aortic lymph nodes, and to assess
to 20 (12.3%); however, node metastasis would have
its potential use in reducing the number of unnecessary
been missed in 20 out of 35 women. On the same basis,
para-aortic lymphadenectomies performed in women with
the number of lymphadenectomies performed would have
ovarian and uterine corpus malignancies, again comparing
been 44 (27.0%) and metastasis would have been missed
its effectiveness with those of preoperative CT and
in 14 women on palpation during surgery, and 71
palpation during surgery.
lymphadenectomies (43.6%) would have been performed
and metastasis would have been missed in three women
on intraoperative ultrasonography. METHODS
Conclusions Intraoperative ultrasonography is a highly According to the protocols of the hospitals in which
sensitive tool with which to diagnose lymph node this study was carried out, pelvic and para-aortic

Correspondence to: Dr E. Ryo, Department of Obstetrics and Gynecology, Teikyo University, 2-11-1, Kaga, Itabashi-ku, Tokyo, 173-8606,
Japan (e-mail: yonchi@med.teikyo-u.ac.jp)
Accepted: 24 March 2008

Copyright  2008 ISUOG. Published by John Wiley & Sons, Ltd. ORIGINAL PAPER
92 Ryo

lymphadenectomy are performed when a woman is less Table 1 Characteristics of the study population
than 75 years old and has a good performance status and
no distant metastasis. Under these conditions, all women Disease Number of patients
with ovarian carcinoma undergo pelvic and para-aortic
lymphadenectomy up to the renal vessels when abdominal Ovarian carcinoma 73
residual tumors are less than 1 cm in diameter. Similarly, FIGO stage
I 33
all women with endometrial carcinoma undergo pelvic II 8
and para-aortic lymphadenectomy up to the renal vessels. III 30
One exception is that para-aortic lymphadenectomy is IV 2
not performed in cases of well-differentiated endometrial Histological study
Serous 26
carcinoma in which no muscular invasion is demonstrated
Mucinous 8
by either preoperative magnetic resonance imaging (MRI) Endometrioid 8
or intraoperative macroscopic findings of the removed Clear 21
uterus. Women with uterine sarcoma also undergo pelvic Other 10
and para-aortic lymphadenectomy when the diagnosis of Endometrial carcinoma 78
sarcoma is confirmed before surgery. FIGO stage
According to these protocols 163 women were recruited I 44
II 10
into this study – 29 consecutive women at Musashino III 23
Red Cross Hospital in 1998–2000, and 134 consecutive IV 1
women at Teikyo University Hospital in 2002–2006 – all Histological study
of whom underwent para-aortic lymphadenectomy. The G1 37
mean age (SD) of the women was 55.6 (± 9.74) years. G2 18
G3 13
There were 73 cases of ovarian carcinoma, 78 cases Other 10
of endometrial carcinoma, seven cases of uterine sar- Synchronous carcinoma 5
coma (six of carcinosarcoma and one of leiomyosarcoma) Uterine sarcoma 7
and five cases of endometrial and ovarian synchronous Total 163
carcinomas. Ten women with ovarian carcinoma under-
FIGO, International Federation of Gynecology and Obstetrics.
went para-aortic lymphadenectomy in interval-debulking
surgery after chemotherapy. No anticancer therapy was
performed before surgery in the remaining 153 women. at least two radiologists, each with more than 10 years’
Table 1 shows the incidence of each type of gynecological experience.
malignancy in the study population. The procedures during surgery were as follows: the
All the women underwent the standard course of woman was placed in the lithotomy position under
treatment usually performed in the participating hospitals, general anesthesia and the lower abdomen was opened
with the only deviation from normal procedure being via a midline incision. After laparotomy the surgeon, who
the addition of intraoperative ultrasonography. All was a gynecological specialist with more than 10 years’
participants gave informed consent, and the study was experience and blinded to the results of the CT scans,
approved by the institutional review board. palpated the para-aortic region and assessed whether
Within 2 weeks before the surgery, CT was performed there were enlarged para-aortic nodes of more than 5 mm
using a helical scanner (Hispeed NX, Lightspeed Plus, in diameter. The para-aortic region was defined as a
GE and Yokogawa Medical Systems, Tokyo, Japan) rectangular area from the level of the aortic bifurcation
in 1999–2000 and a multidetector-row eight-channel to that of the left renal vein and laterally from 6 cm to
helical CT unit (Light Speed QX/I, GE Medical Systems, the right to 3 cm to the left of the aorta. The surgeon
Milwaukee, WI, USA) in 2002–2006. Transverse images could recognize the aorta but not the left renal vein by
5 mm in thickness were obtained at 5-mm intervals at palpation; therefore its level was set at about 5 cm up
the level between the aortic bifurcation and renal vessels. from the lower pole of the left kidney.
All the women received 2 mL/kg nonionic intravenously Next, an examiner, also blinded to the results
administered contrast material at a rate of 2–2.5 mL/s in of the CT and palpation, inserted an intraoperative
1999–2000 (Optiray 320, Yamonouchi, Tokyo, Japan) ultrasound probe into the lower abdominal incision
and 1.5 mL/s in 2002–2006 (Omnipaque, Daiichi, Tokyo, towards the upper abdomen. By making contact with
Japan). Scanning was performed 90–120 s after the the retroperitoneum, the examiner scanned the para-
initiation of intravenous contrast administration. A aortic region, and assessed enlarged nodes. First, the
structure adjacent to the aorta or vena cava was identified para-aortic region was delineated by identifying the aortic
as an enlarged node if it had a well-defined round shape bifurcation, the renal arteries and veins, and the bilateral
with soft-tissue attenuation and its diameter was more ovarian veins that could be visualized on intraoperative
than 5 mm (a previous CT imaging study2 had found that ultrasonography. Then, the left lateroaortic area was
normal nodes at the upper and lower para-aortic regions scanned by moving the ultrasound probe from the aortic
had mean diameters (± SD) of 3.7 (± 0.2) and 3.4 (± 0.1) bifurcation to the renal vessels in the transverse plane.
mm, respectively). These assessments were performed by In the same way, the preaortic and retroaortic areas,

Copyright  2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 32: 91–96.
Intraoperative US for aortic node diagnosis 93

intra-aortocaval area, precaval and retrocaval areas, and A total of 35 women had actual node metastasis.
right laterocaval area were scanned. If a hypoechoic, Enlarged para-aortic lymph nodes were detected on
well-defined and apparently round structure was found, CT in 20 women, of whom 15 had metastasized
its shape was confirmed by further observations from nodes; 20 women had metastasized para-aortic nodes
more than two different directions to exclude vessels. A that were not identified as enlarged on CT. If para-
hypoechoic well-defined round structure adjacent to the aortic lymphadenectomy had been performed only when
aorta or the vena cava was identified as a lymph node, and enlarged lymph nodes were detected on CT, the number
it was assessed as enlarged if its diameter in the transverse performed could have been reduced from 163 to 20
plane was more than 5 mm. All ultrasound scans were (12.3%); however, metastatic nodes would have been
performed by one examiner, who was an ultrasound missed in 20 out of 35 women. Similarly, enlarged
specialist, using an SSD-2000 machine with a UST-995- nodes were palpated in 44 women during surgery,
7.5-MHz probe (Aloka, Tokyo, Japan) in 1999–2000 and and metastatic nodes were found in 21 of these.
a NEMIO SSA 550A machine with a PVF-738H probe Intraoperative ultrasonography detected enlarged nodes
(Toshiba Medical System, Tokyo, Japan) in 2002–2006. in 71 women, of whom 32 had metastatic nodes. If
Following the lower abdominal procedures including para-aortic lymphadenectomy had been performed only
pelvic lymphadenectomy, the abdominal incision was when enlarged lymph nodes were detected, the number
extended to the subxyphoidal region. We mobilized the performed would have been 44 (27.0%) and metastasis
ascending colon, descending colon, and duodenum, and would have been missed in 14 women on palpation, while
displaced them to the right, to the left and upwards, the number performed would have been 71 (43.6%) and
respectively, so that the para-aortic retroperitoneal space metastasis would have been missed in three women on
was opened up to the renal vessels. Lymphatic tissue intraoperative ultrasonography.
surrounding the retroperitoneal vessels was removed
completely and was microscopically examined for node
DISCUSSION
metastasis by pathologists in the hospitals.
It would have been difficult to correlate the results According to the International Federation of Gynecology
obtained for each individual node as evaluated by CT, and Obstetrics surgical staging criteria, patients with
palpation, intraoperative ultrasonography and pathologi- ovarian or endometrial cancer and with positive para-
cal examination. Therefore, just the relationships between aortic lymph nodes are classified as Stage IIIC. However,
the detection of enlarged nodes by each of the three there is no agreement as to how to assess the lymph node
assessment methods and the presence of para-aortic node status.
metastasis, as assessed by pathological examination, in Tempany et al.3 compared ultrasonography, MRI
each woman were examined. The sensitivity, specificity, and CT for staging advanced ovarian cancer, and all
and positive and negative predictive values (PPV and three modalities had relatively high specificities but
NPV) for each assessment method were calculated and only mediocre sensitivities for para-aortic lymph node
compared using the Chi-square test. The potential clinical metastasis. Similar results were obtained by Ozalp et al.4 ,
usefulness of the three assessments in decreasing the num- who compared lymphoscintigraphy, Ga-67 scintigraphy
ber of para-aortic lymphadenectomies performed, while and CT. The current prevailing notion is that enlarged
maintaining high sensitivity for node metastasis, was then lymph nodes must be palpated and resected if necessary.
evaluated. However, several lines of evidence suggest that the results
of intraoperative palpation are frequently incorrect5 – 7 .
Thus clinicomorphological factors and palpation at
RESULTS surgery cannot be relied upon to predict the lymph
node status. Young et al.8 reported that incomplete
Scanning by intraoperative ultrasonography took less than surgical procedures often caused inadequate down
5 min and had no adverse effect on any woman. The mean staging in ovarian cancer, and Trimbos et al.9 reported
(± SD) number of para-aortic nodes removed per woman that complete surgical staging with lymphadenectomy
was 25.6 (± 12.90). Para-aortic lymph node metastasis improved the prognosis of early ovarian cancer. However,
was found microscopically in 18 women with ovarian systematic lymphadenectomy is not yet regarded as
carcinoma, 15 women with endometrial carcinoma, and the standard surgical procedure because it increases
two women with uterine sarcoma. The number of positive surgical morbidity and its therapeutic significance is
nodes per woman showing node metastasis was 4.6 uncertain. There have been several reports suggesting
(± 7.0). Figure 1 shows examples of enlarged nodes that lymphadenectomy improves the prognosis for
detected by intraoperative ultrasonography in two women women with ovarian carcinoma9 – 11 , but others remain
with para-aortic node metastasis. unconvinced12,13 . Panici et al.14 carried out a prospective
Table 2 shows the sensitivity, specificity, PPV and randomized study of women with optimally debulked
NPV of CT, palpation during surgery and intraoperative advanced ovarian carcinoma, and reported that systematic
ultrasonography for the detection of para-aortic lymph lymphadenectomy improved progression-free but not
node metastasis and Table 3 shows the P-values for pair- overall survival compared to the resection of bulky nodes
wise comparisons of the modalities. only.

Copyright  2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 32: 91–96.
94 Ryo

Lymph node

Vena cava
Aorta

Vertebra

Aorta Left renal artery

Lymph node

Vertebra

Figure 1 Intraoperative ultrasound images (transverse sections) showing lymph node 9 mm in diameter located in the intra-aortocaval area
(a), and lymph node 22 mm in diameter located in the left lateroaortic area (b). Computed tomography and palpation could detect the
lymph node shown in (b), but not that in (a).

Table 2 Sensitivity, specificity and positive and negative predictive values (PPV and NPV) of computed tomography, palpation during
surgery, and intraoperative ultrasonography for the detection of para-aortic lymph node metastasis

Method Sensitivity (% (n)) Specificity (% (n)) PPV (% (n)) NPV (% (n))

Computed tomography 42.9 (15/35) 96.1 (123/128) 75.0 (15/20) 86.0 (123/143)
Palpation 60.0 (21/35) 82.0 (105/128) 47.7 (21/44) 88.2 (105/119)
Intraoperative ultrasonography 91.4 (32/35) 69.5 (89/128) 45.1 (32/71) 96.7 (89/92)

The situation for endometrial carcinoma is similar to lymphadenectomy should be performed, and preoperative
that for ovarian carcinoma. A study by the Gynecologic imaging assessments have been reported to be a poor
Oncology Group15 stated that palpation of the nodal predictor of nodal disease4,16 – 18 . In many hospitals patho-
area should not be relied upon to determine whether logical factors guide clinicians in their decision as to

Copyright  2008 ISUOG. Published by John Wiley & Sons, Ltd. Ultrasound Obstet Gynecol 2008; 32: 91–96.
Intraoperative US for aortic node diagnosis 95

Table 3 P-values for pairwise comparisons of modalities this, and the intraoperative approach makes it possible. In
daily clinical practice, most gynecologists are convinced
Modality of the superiority of transvaginal ultrasonography over
pair Sensitivity Specificity PPV NPV the other imaging modalities in observations of the uterus
and ovaries near the vagina. Para-aortic areas are flat and
CT vs. Palp 0.2318 0.0007 0.0773 0.7278
the branching pattern of the vessels is simple compared
IU vs. CT < 0.0001 < 0.0001 0.0344 0.0133
IU vs. Palp 0.0053 0.0286 0.9307 0.0458 with that of the intrapelvic cavity. In some cases, color
Doppler imaging is useful for making a distinction
CT, computed tomography; IU, intraoperative ultrasonography; between lymph nodes and vessels by observing blood
NPV, negative predictive value; Palp, palpation; PPV, positive flow in the latter. Para-aortic lymph nodes are therefore
predictive value. suited to observation by intraoperative ultrasonography.
The diagnostic accuracy of an examination depends
whether or not to remove nodes. Also, in the hospitals upon the criteria that are used. However, when a new
participating in this study, para-aortic lymphadenectomy method is being tested there are initially no data available
is not performed in cases of well-differentiated endome- on which to base a decision as to the criteria that should
trial carcinoma in which no muscular invasion has been be used. In this study, a lymph node was defined as
demonstrated. However, only a few women fit these con- abnormal simply when its diameter in the transverse plane
ditions. Moreover, preoperative pathological findings and was more than 5 mm, a value that was based upon data
macroscopic impression of muscular invasion sometimes from a CT imaging study2 . This cut-off level appears to be
differ from the final pathological diagnosis. Only sys- relatively effective, judging from the results of this study.
tematic lymphadenectomy is an accurate method for Obtaining further imaging data, such as size, number,
evaluating nodal status, but it is not the standard pro- shape and internal echo of lymph nodes, would allow
cedure in endometrial carcinoma. Several reports have better criteria to be established for diagnosing lymph
suggested that lymphadenectomy improves the prognosis node metastasis.
for women with endometrial carcinoma19 – 24 , but this has In conclusion, intraoperative ultrasonography can
been disputed25,26 . detect node metastasis with high sensitivity, allowing
In summary, the assessment of para-aortic lymph nodes avoidance of unnecessary para-aortic lymphadenectomy
is very important in determining the spread of ovarian in women with ovarian and uterine corpus malignancy.
and endometrial carcinoma, but there is no reliable
procedure for doing this other than lymphadenectomy, the ACKNOWLEDGMENTS
therapeutic significance of which is uncertain. Moreover,
it increases operating time and blood loss14 , and I would like to thank Toshiharu Yasugi, Katsumi Mizutani
sometimes causes complications such as para-aortic lymph (Tokyo Metropolitan Komagome Hospital), Shigeki
cyst, chylous ascites and bowel complications. Therefore, Takeshita, Takuya Ayabe (Teikyo University), Yuji
it would be better to have some criteria for the selection Taketani (Tokyo University) and my other colleagues,
of only those women who actually require para-aortic without whose help this work would not have been
lymphadenectomy. possible.
In this study, both specificity and PPV were highest for
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