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Value of Ultrasonically Guided Needle
Biopsy of Pleural Masses:
An Under-Utilized Technique
Wu-Huei Hsu, MD,1,4 Chi-Der Chiang, MD,1 Jeng-Yuan Hsu, MD,1
Chih-Yi Chen, MD,2 Chun-Shih Chiang, MD,1 Tain Lee, MD3
1
Division of Chest Medicine, Department of Internal Medicine, Taichung Veterans
General Hospital, Taichung, Taiwan, R.O.C.
2
Division of Thoracic Surgery, Department of Surgery, Taichung Veterans General
Hospital, Taichung, Taiwan, ROC
3
Department of Radiology, Taichung Veterans General Hospital, Taichung,
Taiwan, ROC
4
National Yang-Ming University, Taipei, Taiwan, ROC
Received 28 December 1995; accepted 5 June 1996
Abstract: Thirty-six patients with pleural masses underwent ultrasonically guided
needle biopsy (UGNB), including ultrasonically guided aspiration biopsy (UGAB) in all
36 patients and ultrasonically guided cutting biopsy (UGCB) in 13 patients. Using
UGAB alone, the diagnostic rate for pleural masses was 64% (23/36); carcinomatous
pleural masses were more easily diagnosed than non-carcinomatous pleural masses
(87% vs 23%, p < 0.01). If both UGAB and UGCB were used, the diagnostic rate was
89% (32/36); thus, selective UGCB was valuable in improving the diagnostic rate of
non-carcinomatous pleural masses (from 23% to 69%). In patients with pleural effusions (n 4 19), 11 underwent cytologic examinations of the pleural effusion (3 also
undergoing pleural biopsy) without conclusive diagnosis; however, the diagnosis was
made from pleural masses by UGAB (n 4 7) or UGCB (n 4 4). In patients without
pleural effusions (n 4 17), 12 had only pleural masses (3 also having multiple peripheral pulmonary nodules and 4 having mediastinal tumors) and could not be diagnosed
by conventional bronchoscopic and sputum examinations. However, the diagnosis was
rapidly confirmed by UGAB (n 4 5) or UGCB (n 4 3) from the pleural masses in 8
patients. We conclude that UGNB is a useful and valuable diagnostic tool, not only
detecting the pleural masses hidden by pleural effusions but also for rapidly diagnosing
the pleural masses. © 1997 John Wiley & Sons, Inc. J Clin Ultrasound 25:119–125,
1997.
Keywords: pleural mass; ultrasonically guided needle biopsy; needle biopsy; cutting
biopsy
Pleural masses, which are frequently caused by
metastatic malignancy and are difficult to diagnose without an image guidance, are occasionally
encountered by chest physicians. Although the
chest radiograph, the most convenient diagnostic
imaging modality for thoracic lesions, is sometimes helpful in the detection of pleural masses, it
is often limited when pleural effusions are present. Therefore, closed pleural biopsy with the
Correspondence to: W.-H. Hsu
© 1997 John Wiley & Sons, Inc.
VOL. 25, NO. 3, MARCH/APRIL 1997
CCC 0091-2751/97/030119-07
Abrams and Cope needles has been widely used to
diagnose pleural effusions of unknown etiologies,
with the diagnostic sensitivity being from 40% to
77%.1–3 Furthermore, even when pleural masses
are found on chest radiographs, the diagnosis is
also limited with conventional bronchoscopic and
sputum examinations. Although fluoroscopy and
computed tomography (CT)-guided percutaneous
needle biopsy have been well documented to be
valuable in the diagnosis of thoracic tumors, the
clinical application of fluoroscopy and CT-guided
percutaneous needle biopsy in diagnosing pleural
masses is less reported and discussed.4–7
119
HSU ET AL.
As is known, ultrasound (US) and ultrasonically guided needle biopsy (UGNB) have been
widely used in the diagnosis of chest wall tumors
and pulmonary and mediastinal tumors abutting
the chest wall, with excellent results.8–12 Nevertheless, similar to the clinical application of fluoroscopy and CT-guided percutaneous needle biopsy, UGNB for pleural masses has not been well
evaluated. Muller et al reported their experience
with the Cope needle under image guidance (fluoroscopy, CT, US) in the biopsy of pleural lesions,
and Chang et al reported their results with the
Tru-Cut needle in performing pleural biopsy under US guidance, yet the results of fine-needle
aspiration biopsy for pleural masses were not
mentioned.13,14 In this article, we describe our experience of using US and UGNB to detect and
diagnose pleural masses, and discuss the value
and necessity of image-guided percutaneous
needle biopsy in the diagnosis of these lesions.
PATIENTS AND METHODS
From April 1990 to December 1993, we prospectively used a US scanner (Toshiba SAL-38B, Tokyo, Japan) with a 3.75 or 4.0 MHz convex or
linear probe to examine admitted patients if the
patients had (1) chest radiographs which revealed
pleural masses, and/or (2) a thoracic CT which
showed pleural masses which were not found on
chest radiographs, and/or (3) chest radiographs
which revealed pleural effusions with a suspicion
of malignancy. The screening of pleural effusions
by US was suggested to evaluate pleural masses
which can be obscured by malignant pleural effusions. If pleural masses were demonstrated by US
and informed consent was obtained from the patients and their families, ultrasonically guided
needle biopsy [UGNB: including ultrasonically
guided aspiration biopsy (UGAB) and/or ultrasonically guided cutting biopsy (UGCB)] was performed to obtain a cytologic and/or histologic diagnosis.8,9,14,15
During this period, 36 patients with pleural
masses undergoing UGNB were enrolled in our
series. Of these, 19 patients had pleural effusions
found in chest radiographs, and the remaining 17
had no pleural effusions. Furthermore, 29 patients also had thoracic CT examinations.
In the enrolled 36 patients, 25 were men and 11
women, ranging in age from 12 years to 78 years,
with a mean of 59 years. Ten had previous underlying diseases, including nasopharyngeal cancer
post-radiotherapy (n 4 2), lung cancer postlobectomy (n 4 1), malignant melanoma postexcision (n 4 1), cervical cancer post-hysterectomy
120
(n 4 1), renal cell carcinoma post-operation (n 4 1),
epithelioid hemangioendothelioma of right arm
post-operation (n 4 1), esophageal cancer postoperation (n 4 1), and pulmonary tuberculosis with
anti-TB chemotherapy (n 4 2). In the following
management, another 5 patients received surgical
interventions, including thoracotomy for 1 tuberculoma and 2 fibrous methotheliomas, thoracoscopic
biopsy for 1 malignant thymoma, and thoracotomy
with surgical biopsy for 1 unresectable lung cancer.
All 36 patients with pleural masses underwent
UGAB and 13 of them also underwent UGCB due to
non-diagnosis in 7, inconclusive diagnosis in 4, and
suspicion of malignant methothelioma in 2 (adenocarcinoma was proven by UGAB).
In the performance of UGNB for pleural
masses, the sonographic appearances of pleural
masses were first printed on sonopapers and
evaluated by measuring the shortest distance
from the skin. After the evaluation was completed
and informed consent was obtained from the patients and their families, UGNB (UGAB and/or
UGCB) was arranged in order to obtain a pathological diagnosis.8,9,14,15 A 21-gauge fine needle
constructed of steel and consisting of an inner stylet and an outer sheath (PTC needle, Tokyo, Japan, 15 cm in length) was first used for UGAB
with a puncture probe having central channel
guidance (4.0 MHz linear puncture probe,
Toshiba, Japan), and a 25 mL syringe connected
to the fine needle for aspiration.8,15
The aspirated specimens were sprayed on glass
slides: some slides were immediately stained by
the modified Papanicolaou’s stain procedure and
checked by clinical doctors; the others were fixed
in 95% ethanol and sent for cytologic examination.8,15 If the slides of Papanicolaou’s stain revealed positive or conclusive findings, the procedure of UGAB was complete; if the slides of
Papanicolaou’s stain were negative or inconclusive, a second or third pass of UGAB was arranged. In situations in which positive or conclusive results were not made after the repeated
UGAB, UGCB, with a 16–18 gauge biopsy needle
(Tru-Cut needle, Top Surgical, Tokyo, Japan) was
carried out, then the specimens obtained from
UGCB were sent for histologic examination.9,15 In
some patients with large tumors and/or pleural
masses located in the supraclavicular region
(when the puncture probe could be used only with
difficulty), UGAB and/or UGCB was performed
directly after US localization.15 Following the performance of UGNB, chest radiographs were usually obtained immediately or within 30 minutes
after the needle biopsies to detect possible complications.
JOURNAL OF CLINICAL ULTRASOUND
NEEDLE BIOPSY OF PLEURAL MASSES
To evaluate the diagnostic results of UGNB in
pleural masses, we divided the pleural masses
into carcinomatous (n 4 23) and non-carcinomatous (n 4 13) groups and compared the diagnostic results.15 In the assessment of US and
UGNB in the detection and diagnosis of pleural
masses, we also divided the patients into two
groups: one group with pleural effusion (n 4 19)
and the other without pleural effusion (n 4 17).
We reviewed and analyzed the clinical examinations in the enrolled 36 patients, including image
evaluations, laboratory studies, and the results of
UGNB. The necessity and value of UGNB in the
diagnosis of pleural masses were also discussed.
Statistical evaluation was carried out using the
chi-square test, and p < 0.05 was considered to
indicate a statistically significant difference.16
RESULTS
Enrolled in our series were 36 patients with pleural masses who had proven pathological diagnoses and compatible clinical conditions during
follow-up. Of these, all patients underwent
UGAB, and 13 of them also underwent UGCB due
to non-diagnosis in 7 [fibrous methothelioma (n 4
2), adenocarcinoma of the lung (n 4 2), malignant
thymoma (n 4 1), renal cell carcinoma (n 4 1),
and tuberculoma (n 4 1)], inconclusive diagnosis
in 4 [suspicion of lymphoma (n 4 2), sarcoma (n
4 1), and malignant thymoma (n 4 1)], and a
suspicion of malignant methothelioma in 2 (adenocarcinoma was proven by UGAB).
Using UGAB alone, the diagnostic rate for
pleural masses was 64% (23/36); obviously carcinomatous pleural masses were more easily diagnosed than non-carcinomatous pleural masses
(87% vs 23%, p < 0.01) (Figure 1). If both UGAB
and selective UGCB were used, the diagnostic
rate was 89% (32/36) (Figure 2); thus, selective
UGCB was valuable in improving the diagnostic
rate of non-carcinomatous pleural masses (from
23% to 69%). The remaining 4 patients, not diagnosed by UGAB and/or UGCB, were finally diagnosed by thoracotomy in 3 [tuberculoma (n 4 1)
and fibrous methothelioma (n 4 2)] and thoracoscopic biopsy in 1 [malignant thymoma (n 4 1)].
The final diagnoses and diagnostic results of
FIGURE 1. (A) Chest radiograph revealed left pleural effusion and multiple pleural masses (arrows). (B) Chest US (through the supraclavicular
approach) showed lobulated, isoechoic, pleural masses (arrowheads). Small cell lung cancer was diagnosed by UGAB (M = mass, L = lung, P =
pleura).
VOL. 25, NO. 3, MARCH 1997
121
HSU ET AL.
UGNB in the 36 pleural masses are given in
Tables 1 and 2. Two patients with the adenocarcinoma diagnosed by UGAB also underwent
UGCB due to a high suspicion of malignant methothelioma. Finally, 1 patient was proven to have a
malignant methothelioma by UGCB and the
other was confirmed to have an adenocarcinoma
of the lung. In our series, no complications developed after UGNB.
Table 3 also shows the findings of the chest
radiographs and thoracic CT scans of the enrolled
36 patients. In patients with pleural effusion (n 4
19), 7 had pleural masses found in their chest
radiographs, and the remaining 12 had only pleural effusions in their chest radiographs. These
pleural masses were detected by US alone (n 4 3)
or CT and US (n 4 9). Interestingly, 11 patients
underwent cytologic examination of their pleural
effusions ranging from one to three times (3 also
undergoing conventional pleural biopsies) without conclusive diagnoses; nevertheless, the diagnoses were confirmed from the pleural masses by
UGAB [n 4 7—lung cancer (n 4 5), nasopharyngeal cancer (n 4 1), and cervical cancer (n 4 1)]
or UGCB [n 4 4—lymphoma (n 4 2), renal cell
carcinoma (n 4 1), and lung cancer (n 4 1)].
Table 4 shows the clinical methods used in diagnosing 19 malignant pleural effusions with pleural masses.
In patients without pleural effusion (n 4 17),
as shown in Table 3, 16 had pleural masses found
in their chest radiographs, and the remaining one
was accidently found to have pleural masses by a
thoracic CT scan. Of these, 12 patients had only
pleural masses (n 4 4), mediastinal tumors and
pleural masses (n 4 4), multiple peripheral pul122
FIGURE 2. This patient had renal cell carcinoma post-operation. He
was admitted to the hospital again due to a non-productive cough and
dyspnea for several weeks. (A) Chest radiograph showing increasing
density of the right lung field (arrow) and atypical pleural effusion. (B)
Thoracic CT scan revealed multiple pleural masses (arrowheads). (C)
Chest US also showed multiple pleural masses, hidden by the pleural
effusion and at the lateral chest wall and diaphragmatic pleura. A
UGAB was performed without definite diagnosis; UGCB was carried
out and renal cell carcinoma was diagnosed (L = liver, D = diaphragm,
M = mass, E = effusion).
JOURNAL OF CLINICAL ULTRASOUND
NEEDLE BIOPSY OF PLEURAL MASSES
TABLE 1
Final Diagnoses and Diagnostic Results of UGAB and UGCB in 36
Pleural Masses
Diagnosis
Diagnosis
by UGAB
(n)
Diagnosis
by UGCB
(n)
Lung cancer (n = 18)
Adenocarcinoma (n = 13)
Squamous cell carcinoma (n = 3)
Small cell carcinoma (n = 2)
Metastatic malignancy (n = 10)
Malignant thymoma (n = 3)
Nasopharyngeal carcinoma (n = 2)
Cervical cancer (n = 1)
Malignant melanoma (n = 1)
Renal cell carcinoma (n = 1)
Epithelioid hemangioendothelioma (n = 1)
Esophageal cancer (n = 1)
Malignant lymphoma (n = 2)
Malignant methothelioma (n = 1)
Fibrous methothelioma (n = 2)
Tuberculosis (n = 3)
16
11
3
2
4
0
2
1
1
0
0
1
0
0
0
2
3 (3)
3 (3)
0
0
4 (4)
2 (2)
0
0
0
1 (1)
1 (1)
0
2 (2)
1 (1)
0 (2)
0 (1)
Total (n = 36)
23
10 (13)
The numbers in parenthesis indicate the patients undergoing UGCB. Four patients underwent surgical interventions, including thoracotomy in three [tuberculoma (n = 2) and fibrous methothelioma (n = 2)] and thoracoscopic biopsy in
one [malignant thymoma (n = 1)]. One patient underwent UGAB and UGCB due
to a high suspicion of malignant methothelioma, but the diagnosis of adenocarcinoma was confirmed.
TABLE 2
Diagnostic Results of UGAB and UGCB in Carcinomatous and
Non-Carcinomatous Pleural Masses
Group
UGAB
UGCB
Total
Carcinomatous (n = 23)
Non-carcinomatous (n = 13)
20/23 (87%)*
3/13 (23%)*
4/4 (100%)
6/9 (67%)
23/23 (100%)
9/13 (69%)
Total (n = 36)
23/36 (64%)
10/13 (77%)
32/36 (89%)
*P < 0.01 by chi-square test.
One patient underwent UGAB and UGCB due to a high suspicion of malignant
methothelioma, but the diagnosis of adenocarcinoma was confirmed.
UGAB = ultrasonically guided aspiration biopsy.
UGCB = ultrasonically guided cutting biopsy.
monary nodules and pleural masses (n 4 3), or no
abnormal findings (n 4 1) in their chest radiographs. Therefore, the diagnosis could not possibly be made by conventional bronchoscopic and
sputum examinations. However, 8 patients had
diagnoses rapidly made from the pleural masses
by UGAB [n 4 5—lung cancer (n 4 1), esophageal cancer (n 4 1), melanoma (n 4 1), and tuberculoma (n 4 2)] or UGCB [n 4 3—malignant
thymoma (n 4 2) and epithelioid hemangioendothelioma (n 4 1)]. The remaining four, as stated
above, were finally diagnosed by surgical intervention.
DISCUSSION
In the detection and diagnosis of pleural masses,
undoubtedly the chest radiograph alone is not
VOL. 25, NO. 3, MARCH 1997
sufficient, as reported in our series and the literature.17 Even when pleural masses are detected by
chest radiographs, it is difficult to obtain a pathological diagnosis by percutaneous needle biopsy under radiographic guidance. Thus, in the diagnosis of
pleural masses, percutaneous needle biopsy using
other imaging systems for guidance, such as fluoroscopy, US, CT, is necessary and helpful.
However, in the review of published literature,
image (fluoroscopy, US, CT)-guided percutaneous
needle biopsy for pleural masses is less reported
and discussed.13,14,17,18 For example, Goerg et al
reported their good results of using US to detect
pleural metastases in 32 patients; however, only
2 patients underwent UGAB.17 The low incidence
of performing percutaneous needle biopsy for
pleural masses may have the following reasons:
123
HSU ET AL.
TABLE 3
Findings of Chest Radiographs and Computed
Tomography in 36 Patients with Pleural Masses
CR
CT
With pleural effusion
Lung tumors + pleural masses
Pleural masses only
Pleural effusion only
Mediastinal tumors + pleural masses
Without pleural effusion
Lung tumors + pleural masses
Multiple lung nodules + pleural masses
Mediastinal tumors + pleural masses
Pulmonary infiltrate + pleural masses
Pleural masses only
Normal
19
2
5
12
0
17
4
3
4
1
4
1*
16
5
9
0
2
13
3
1
4
0
5*
0
Total
36
29
*This patient had esophageal cancer post-operation. Chest radiograph revealed no lung lesions, but thoracic CT showed pleural
masses.
CR = chest radiograph. CT = computed tomography.
TABLE 4
Methods Used in Diagnosing 19 Malignant
Pleural Effusions
Diagnostic
Method
Conventional methods
Cytologic examination of
pleural effusion (n = 11)
Blind pleural biopsy (n = 3)
US-guided needle biopsy of
pleural masses
UGAB (n = 19)
UGCB (n = 5)
Proven Malignant
Pleural Effusion
Positive
Negative
0
0
11
3
15
5
4
0
Three patients underwent cytologic examinations of pleural effusions, blind pleural biopsies and UGAB; however, no conclusive diagnosis was made. Confirmative diagnoses were made by UGCB
from the pleural masses.
One patient was misdiagnosed as adenocarcinoma by UGAB, but
malignant methothelioma was proven by UGCB.
(1) in patients with pleural effusions and pleural masses, pleural masses can’t be found by fluoroscopy, and the closed pleural biopsy and cytologic examination of malignant pleural effusions
has a diagnostic accuracy ranging from 48% to
65%1–3,19–21; (2) in cases where the pleural biopsies and cytologic examinations give negative results, thoracoscopy is often carried out; (3) with
multiple pleural masses, this condition is often
caused by metastases from underlying primary or
unknown malignancies (representing a terminal
stage), and the pathological diagnosis is not
strongly indicated; (4) in patients who are suspected of having primary fibrous methothelioma,
surgical resection is first considered.
Clinically, in the evaluation of pleural masses, is
124
it always necessary and indicated to perform the
image-guided percutaneous needle biopsy? In our
series, some advantages were still found after
UGNB for the pleural masses. For example, in our
patients without pleural effusions, metastatic lung
malignancy was strongly suspected in one patient
from the chest radiographs which revealed multiple
lung nodules and pleural lesions, but tuberculosis
was confirmed by UGAB from the pleural mass.
Furthermore, some patients with pleural masses,
impossible to be diagnosed by conventional bronchoscopic and sputum examinations, could be rapidly diagnosed by UGNB; thus eliminating the need
for invasive diagnostic procedures, such as thoracotomy, mediastinoscopy and thoracoscopy. In our
patients with pleural effusions, as shown in Table
4, 11 patients had both UGNB for pleural masses
and cytologic examination of the pleural effusions.
Accidentally and interestingly, all results of UGNB
were positive, but the cytologic results of the pleural
effusion evaluations were negative.19–21 From these
results, we suggest that US and UGNB can increase the diagnostic rates for pleural masses and
shorten the time to pathological diagnosis as well as
patients’ admissions. Practically, we have recently
performed UGNB to diagnose pleural masses first
when the pleural masses were found by chest radiograph, CT, or US.
In considering UGAB and UGCB for diagnosing
pleural masses, we suggest UGAB as the first
choice and selective UGCB if necessary. As shown
in Table 2, carcinomatous pleural masses can be
more easily diagnosed by UGAB than non-carcinomatous pleural masses (87% vs 23%, p < 0.01);
moreover, selective UGCB can improve the diagnostic results of UGNB in non-carcinomatous pleural masses (from 23% to 69%). Although some
authors think the interpretations of aspirated
specimens may be variable (an experienced cytopathologist often makes a definite diagnosis without
difficulty), there is no doubt that small aspirated
specimens sometimes make the diagnosis difficult,
especially when specimens are aspirated from benign or noncarcinomatous tumors.4,7,9,10,22
Regarding the complications of UGNB in thoracic lesions, minimal complications are occasionally reported in published papers, such as pneumothorax, hemoptysis.8–10,14,22 For image-guided
needle biopsy in the diagnosis of pleural masses,
only pneumothorax has been reported.13,14 However, in our series, no complications occurred using UGNB to biopsy pleural masses. Pleural
masses often occurred in the parietal pleura and
were not influenced by respiratory movement,
which decreased and prevented the occurrence of
complications.12
JOURNAL OF CLINICAL ULTRASOUND
NEEDLE BIOPSY OF PLEURAL MASSES
Among image (fluoroscopy, CT, US)-guided
percutaneous needle biopsy used in the diagnosis
of thoracic lesions, fluoroscopy and CT-guided
percutaneous needle biopsy have been well established as valuable methods with excellent diagnostic results, whereas US and UGNB were only
applied in thoracic lesions abutting the chest
wall.4–14 Furthermore, CT and CT-guided percutaneous needle biopsy not only show the whole
thoracic lesion in detail but also can biopsy the
difficult thoracic lesions.5,6 However, in evaluating pleural masses, US still has some advantages
over CT and fluoroscopy in detecting and diagnosing pleural masses: (1) rapid and convenient (US
and UGNB can be arranged at bedside, whereas a
fluoroscopic and CT-guided needle biopsy might
be difficult or impossible), (2) detecting the pleural masses in real-time and making needle biopsies simultaneously, and (3) no radiation exposure. Practically, some patients with pleural
masses and pleural effusions often had complaints of dyspnea and chronic cough21; therefore,
it was difficult or impossible for these patients to
lie in bed for a thoracic CT examination or fluoroscopic and CT-guided needle biopsies.
In conclusion, pleural masses are sometimes encountered by chest physicians and are usually difficult to diagnose by chest radiographs alone. To
detect and diagnose pleural masses, image (fluoroscopy, CT, US)-guided percutaneous needle biopsy is
helpful and necessary. However, fluoroscopic and
CT-guided percutaneous needle biopsies are occasionally inconvenient and time-consuming, especially when patients have pleural effusions and are
dyspneic. Chest US can serve as a combination of
detection and diagnosis methods, with UGNB performed simultaneously and easily. In our experience, the performance of UGNB is convenient,
rapid, and safe. We strongly recommend the use of
US and UGNB to detect and diagnose pleural
masses, especially when malignant pleural effusions are highly suspected and undiagnosed.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
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