Initial experience with a new laparoscopic ultrasound probefor guided biopsy in the staging of upper gastrointestinal cancer

Hazem Hassan Æ Peter Vilmann Æ Vijay Sharma ÆJakob Holm

Received: 5 August 2008 / Accepted: 7 December 2008 / Published online: 5 March 2009

� Springer Science+Business Media, LLC 2009

Abstract

Background Until recently, laparoscopic ultrasound

(LUS)-guided biopsy has been difficult with the available

probes on the market. This study aimed to present a new

laparoscopic ultrasound probe (Hitachi, EUP-OL531) for

guided biopsy and describe its impact on the clinical out-

come for patients with upper gastrointestinal (UGI) cancer.

Methods Patients referred with confirmed UGI cancer from

June 2003 to December 2006 were included in the study.

After a standard workup including computed tomography,

endoscopic ultrasound, and ultrasound of the neck, operable

patients underwent LUS with or without fine-needle aspira-

tion (FNA).

Results From a total of 175 patients, 19 (11%) underwent

LUS-guided FNA after a significant lesion was found. The

LUS-guided FNA confirmed distant metastasis in 14 of the

19 patients and changed the clinical management for these

14 patients (8%). There were no adverse events due to LUS

or LUS-guided FNA.

Conclusion The current results with the new LUS probe

for guided FNA are encouraging in terms of its diagnostic

ability, safety, and ease of use.

Keywords Fine-needle aspiration �Laparoscopic staging � Laparoscopic ultrasound �LUS � LUS-FNA � Upper GI cancer

Accurate staging of upper gastrointestinal tract (UGI)

neoplasms remains a challenge. Because survival is closely

related to the tumor node metastasis (TNM) stage, a range

of different methods is used to achieve an exact prethera-

peutic staging evaluation including computer tomography

(CT), transabdominal ultrasound (TUS), endoscopic ultra-

sound (EUS), angiography, magnetic resonance (MR), and

positron emission tomography (PET). Unfortunately, these

methods are not sufficiently accurate when used either

alone or in combination.

Since the past decade, laparoscopic staging has been

added to avoid unnecessary laparotomies, changing the

management of these malignancies. In recent years, an

increasing number of papers have discussed the role of

intraoperative ultrasound during laparoscopic staging and

its accuracy in detecting regional and distal metastases

[1–4]. Laparoscopic ultrasonography (LUS) represents a step

forward in evaluation of the abdominal cavity, allowing

detection of lesions such as locally advanced disease and

dissemination that otherwise would be overlooked and thus

improving the sensitivity of tumor staging [5].

Currently, several types of LUS probes are used. Most

have a linear-array transducer mounted on a flexible probe

with a frequency range of 4.0 to 10.0 MHz. These LUS

probes allow detection of lesions suspicious of malignancy

such as small liver lesions, suspicious lesions in other

organs, and suspicious lymph nodes, but samples of tissue

are needed to confirm the disease progression.

Until recently, LUS-guided biopsy has been a difficult

and cumbersome, if not impossible, maneuver with the

probes available on the market [6]. The needle has to be

introduced through the anterior abdominal wall, and free-

hand guidance with the transducer must be performed

[4–6]. Alternatively, as described with the B and K probe

[6], the needle must pass through an exterior floppy biopsy

sheath before initiation of the biopsy maneuver [7, 8].

This study aimed to present a new prototype LUS probe

for guided biopsy (Hitachi, EUP-OL531, Hitachi Medical

H. Hassan (&) � P. Vilmann � V. Sharma � J. Holm

Gentofte Hospital, Copenhagen, Denmark

e-mail: hazim@dadlnet.dk

123

Surg Endosc (2009) 23:1552–1558

DOI 10.1007/s00464-009-0336-3

Corporation, Tokyo, Japan) and to investigate the impact of

LUS-guided fine-needle aspiration (FNA) with the new

probe on the clinical outcome for patients with UGI cancers.

Material and methods

This prospective pilot study was conducted from 1 June

2003 to 31 December 2006. The study included patients

referred to the department of surgical gastroenterology at

Gentofte University Hospital with confirmed esophageal,

gastroesophageal (GE) junction, and gastric cancer.

The patients underwent preoperative staging according

to a standard protocol. They initially were interviewed as

outpatients by one of the surgeons in the department, who

obtained a case history and clinical assessment. The

patients were offered prescheduled dates for EUS, com-

puted tomography (CT) of the thorax and abdomen, and

ultrasound of the neck for detection of suspicious lymph

nodes. At this interview, relevant information regarding

different investigative procedures including risks, compli-

cations, and informed consent was obtained.

A second evaluating interview was held to review the

results of the aforementioned investigations. If no signs of

inoperability were observed at this point, the patients were

offered diagnostic laparoscopy and LUS in one session,

with eventual LUS-guided FNA if relevant. The LUS

evaluation was performed as a separate procedure and not

in connection with surgery. Patients with signs of inoper-

ability were referred for palliative therapy including

oncologic treatment and palliative endoscopic procedures

such as enteral stent placement.

The following information was gathered for each

patient: age, sex, type of primary cancer (gastric, GE

junction, or esophageal), histology reports, EUS findings,

EUS-guided FNA cytology, CT of the thorax and abdomen,

ultrasound of the neck, laparoscopy, LUS, and LUS-guided

FNA cytology. Other radiologic procedures, type of ther-

apy (radical or palliative), follow-up evaluation, and final

pathology diagnosis also were recorded.

To study the impact of LUS-guided FNA biopsy on the

clinical outcome for patients with esophageal and gastric

cancer, the history of each patient and the radiologic

findings were reviewed up to the referral for LUS. A board

of two surgeons (P. Vilmann and H. Hassan) decided on the

further course for the patient if a LUS and FNA had not

been available and compared it with the actual clinical

management after LUS.

Equipment and setting

The LUS probe (Hitachi OL 531) (Fig. 1) was developed

by one of the authors (P. Vilmann) and the Hitachi

Company in collaboration. The probe has a diameter of

11.8 mm and fits into a 12-mm port. The total length of the

instrument is 67 cm, and the length of the insertion tube is

42 cm. There is an electronic transducer that has a scan-

ning angle of 608 with a lateral and slight oblique forward

view (Fig. 2). The curve radius is 10 mm. The center fre-

quency is 7.5 MHz with a bandwidth of 5 to 10 MHz. The

transducer mounted at the flexible tip of the instrument can

be moved 908 up and down and left and right. A removable

metal needle cover case around the body of the probe shaft

forms a 3.2-mm biopsy channel. This channel can be

reduced to 2.4 mm with a mountable inner plastic tube

(Fig. 3A, B), allowing a modified 22- or 19-gauge aspira-

tion biopsy needle (Sonotip II; Medi-Globe Corp.,

Achenmuhle, Germany) (Figs. 3B, 4). The probe can be

connected to a Hitachi ultrasound scanner (EUB 6500 or

EUB 8500) with power and color Doppler facilities as well

as elastography. The probe can be fully sterilized in

STERRAT (H2O2 plasma) or with the use of ethylene

oxide gas sterilization. A picture-in-picture function and a

fully emersible remote control for image adjustment also

have been developed.

Fig. 1 The new laparoscopic ultrasound probe (Hitachi OL 531)

Fig. 2 Probe that has an electronic curved array transducer with a

scanning angle of 608 mounted at its end. A needle is extending from

the biopsy channel end

Surg Endosc (2009) 23:1552–1558 1553

123

Examination procedure

The procedure was performed with the patient under gen-

eral anesthesia. The presetting of the image direction was

as usual, with distal to the right and proximal to the left in

the ultrasonic image. This gives images very similar to the

EUS images obtained with linear transducers. For staging

of the upper gastrointestinal (GI) cancer, the author pre-

ferred the left upper quadrant and the supraumbilical port

because it gives a good access to the left liver lobe, the

region of the cardia, the hepatoduodenal ligament in a

longitudinal scanning direction, and the pancreas in a

horizontal section. The aorta and the celiac vessels could

be seen from the umbilical port, and the right liver lobe

could be examined as well. The LUS procedure was per-

formed in a systematic way including all segments of the

liver, the hepatoduodenal ligament, the celiac trunk, the

superior mesenteric artery, the adrenals, and, if relevant,

the pancreas.

The branches of the celiac axis, the portal vein, the

superior mesenteric artery, and the aorta were displayed in

transverse sections from the left subcostal trocar. The

lymph nodes along these vessels were classified according to

the tumor node metastasis (TNM) classification. Metastatic

lymph node involvement was most likely characterized by

a hypoechoic pattern, round shape, and well-delineated

boundaries.

Color Doppler examination was performed to delineate

the vascular anatomy and to distinguish vessels from

lymph nodes. Biopsy of lymph nodes was done if consid-

ered relevant (i.e., for a change in management of a patient

found positive for malignancy).

FNA biopsy procedure

After a lesion had been outlined, the needle was simply

introduced via the biopsy inlet of the probe and firmly

connected to the luer-lock biopsy inlet (Fig. 3B). The stylet

was withdrawn a few millimeters, and the needle was

advanced under ultrasonic guidance directly into the lesion

(Fig. 5). Then the stylet was removed completely, and

vacuum was applied to the needle with a 10-ml syringe.

To-and-fro movements were performed under ultrasonic

guidance. The entire biopsy needle instrument finally was

removed. The material was expelled onto glass slides and

smeared for a cytologic evaluation.

Results

A total of 363 patients with UGI cancer were referred for

preoperative staging: 80 patients with gastric cancer (22%),

163 patients with GE junction cancer (45%), and 120

patients with esophageal cancer (33%)). A full preoperative

staging program, including LUS, was offered to 175 (48%)

of the patients. The remaining 188 patients (52%) either

were found to be inoperable at an early stage in the staging

program or were, due to logistical matters, offered the same

program including diagnostic laparoscopy without LUS.

The staging program could not include LUS for every

patient because only three surgeons were trained to per-

form the LUS procedure.

Of the 175 patients undergoing LUS, 19 (2 women and

17 men) (11%) underwent LUS plus LUS-guided FNA.

The LUS-FNA procedure could easily be performed in all

cases with the new LUS probe. The findings showed that

Fig. 3 a Biopsy channel reduced to 2.4 mm with a mountable inner

plastic tube. b The LUS probe fully assembled with a biopsy needle

mounted and ready to use

Fig. 4 A modified 22-gauge aspiration biopsy needle (Sonotip II;

Medi-Globe Corp., Achenmuhle, Germany)

1554 Surg Endosc (2009) 23:1552–1558

123

11 patients had GE-junction cancer (58%), 3 patients had

gastric cancer (16%), and 5 patients had esophageal cancer

(26%). For 16 of the 19 patients, the pathology of the

primary tumor was adenocarcinoma (84%), and for the

remaining 3 patients, the pathology was squamous cell

carcinoma (16%). The demographic data and workup

details can be seen in Table 1.

Of the 19 FNA biopsies taken (size, 18 mm; range, 5–

30 mm), 15 (79%) demonstrated malignant cytology and 4

(21%) were benign. Of the 15 patients with malignant

cytology, 10 (67%) underwent FNA biopsies from sus-

pected lesions in the liver, 2 (13%) had a FNA taken from

enlarged lymph nodes adjacent to the left gastric artery, 3

(20%) had a FNA taken from enlarged lymph nodes

adjacent to the celiac trunk, and 1 (6.7%) had a FNA taken

from both adrenal glands.

For only 6 of the 19 patients (31%), CT scan demon-

strated suspicious lesions in the liver, but no biopsy

verification was performed for these patients before the

LUS procedure. For 14 patients (74%), LUS-guided biopsy

diagnosed cancer spread compatible with a distant metas-

tasis. All 14 patients with distant metastasis received

palliative therapy (chemoradiotherapy with or without

enteral stenting), and unnecessary surgery was avoided.

One patient with localized disease received palliative

treatment because of old age and comorbidity. Another

patient who had resectable disease with a liver lesion FNA

suggestive of cirrhosis also was not referred for final sur-

gery due to a high surgical risk. For 14 patients (8%) in a

total of 175, LUS with FNA changed the outcome, with

upper GI cancers referred. No complication was recorded

for the 175 patients undergoing diagnostic laparoscopy-

LUS with or without guided FNA.

Three of the four patients with benign LUS-guided FNA

biopsies went for curable surgery with or without periop-

erative chemotherapy. One patient with a benign FNA was

not fit for surgery at the time of the final evaluation due to

deterioration of his general condition, and was offered

palliative chemotherapy.

Discussion

The current staging workup of patients with UGI cancer is

aimed at assessing the depth of wall penetration, lymphatic

spread, and systemic metastases [6]. Recent advances have

made diagnostic laparoscopy an even more complete

staging tool for gastrointestinal malignancies. These

advances include LUS with a flexible ultrasound probe and

diagnostic lavage to search for free tumor cells in the

abdominal cavity [7, 8]. Staging laparoscopy using lapa-

roscopy and LUS has proved to have an accuracy of about

75% to 83% in assessing the resectability of upper GI

malignancy [2]. As a safe and minimally invasive proce-

dure with low morbidity and no mortality, it is considered

as a valuable staging method, complementing conventional

staging investigations (chest X-ray, ultrasound of the

abdomen, ultrasound of the neck, CT, and EUS).

Fig. 5 Needle advanced under

ultrasonic guidance directly into

a lesion outlined during

laparoscopic ultrasound (LUS).

A liver metastasis of 10 mm

was targeted. Note the

reflections from the needle

inside the lesion

Surg Endosc (2009) 23:1552–1558 1555

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1556 Surg Endosc (2009) 23:1552–1558

123

Mortensen et al. [9] used new dedicated needles for

LUS-guided FNA and histologic biopsies and reported

additional findings in up to 49% of patients. According to

their results CT, ultrasound, and laparoscopy detected 50%

of the nonresectable patients; EUS alone found 79%; and a

combination of EUS and LUS-guided FNA detected all

nonresectable patients. In a study of 420 patients with a

resectable tumor after conventional staging, Dijkum et al.

[10] found that the combination of laparoscopy and LUS

could prove metastatic disease and prevent unnecessary

laparotomies for 20% of patients, with a range of 5% to

40% depending of the type of tumor.

In the current study, LUS and LUS-guided FNA were

able to detect an additional 8% of the patients with

incurable disease, all of whom were considered candidates

for surgery by other investigations, and hence were able to

prevent unnecessary morbid surgery for these patients.

From a study of 127 patients who had adenocarcinoma of

the esophagus or cardia without evidence of metastatic

spread, Stein et al. [11] reported that laparoscopy and LUS

showed 22% to have liver metastases and 25% to have

peritoneal metastases. The same results could not be con-

firmed for squamous cell carcinoma. Conlon et al. [12]

reported that laparoscopy and LUS found 92 patients with

gastric cancer to have metastatic disease that was unap-

preciated by conventional staging methods in one-third of

the patients.

Hepatic metastases in patients with carcinoma of the

esophagus or cardia are associated with a dismal prog-

nosis. Exact knowledge of their presence or absence

is therefore essential before any extensive therapeutic

approach is considered. Current methods for detecting

liver metastases include percutaneous ultrasound, CT, and

MRI. However, even with modern technology, liver

metastases smaller than 1 cm cannot be reliably detected

by means of these techniques [13]. Liver metastases

smaller than 0.5 cm can be seen with laparoscopy if they

are located at the hepatic surface, whereas close contact of

the LUS probe with the hepatic surface allows detection of

previously unknown metastases deep within the hepatic

parenchyma.

In the current study, we detected liver metastases

ranging in size from 5 to 30 mm in 10 patients. With the

use of CT scan, liver lesions suggestive of metastasis

without histologic proof were demonstrated in only half of

the patients. Other studies also have reported diagnosis of

previously unknown hepatic metastases in patients with

advanced gastric carcinoma who are undergoing diagnostic

laparoscopy and ultrasound [7, 11, 14, 15].

Tumor invasion of the celiac axis lymph nodes play a

dominant prognostic role for patients with carcinoma of the

esophagus or cardia [6]. In the current study, assessment of

the celiac axis region with a flexible LUS probe and a new

FNA device was superior to percutaneous ultrasound- or

CT-guided biopsy in the diagnosis of celiac axis lymph

node metastases.

For patients advanced carcinoma of the esophagus and

GE junction, tumor stenosis precludes EUS evaluation

below the stenosis. In our study, 6 of 19 patients had ste-

nosis that prevented a complete EUS evaluation. The use of

LUS with FNA showed a liver metastasis in four patients, a

celiac lymph node metastasis in two patients, and an

adrenal metastasis in one patient diagnosed.

A study by Catheline et al. [16] showed that pancreatic

cancer associated with liver metastases, nodal spread,

peritoneal spread, and venous invasion also could be

diagnosed with high sensitivity (range, 90–100%) using

laparoscopy and LUS. Hunerbein et al. [17] reported that

LUS proved to give additional information in cases of

esophageal, gastric, and pancreatic cancer at respective

rates of 52%, 20%, and 10%.

Currently, only needles for fine-needle biopsy have been

developed for the present probe (Hitachi OL 531), whereas

a true-cut histologic needle is commercially available for

the B and K probe. It is only a matter of time before a

histologic needle is available for the Hitachi probe also.

Conclusion

The current results with the new LUS probe for guided

FNA are encouraging in terms of its diagnostic ability,

safety, and ease of use. We expect that this probe will find

an important place in the preoperative staging evaluation of

patients with upper GI cancer.

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