Thoracic Jung-Gi Chu-Wan

Im, MD #{149} Man Chung Han, MD Kim, MD #{149} Jong Wook Seo, MD

Lobar Bronchioloalveolar ‘ ‘Angiogram Sign The authors reviewed computed tomographic (CT) scans of 12 patients with lobar bronchioloalveolar carcinoma. Seven patients had consolidation of the entire lobe, and five patients had segmental consolidation. After contrast material was administered intravenously, the consolidated lung typically appeared on the scan as an area of homogeneous low attenuation, within which were enhanced branching pulmonary vessels (the CT angiogram sign). To evaluate the specificity of this sign in the discrimination of bronchioloalveolar carcinoma, CT scans of 26 patients who had lobar consolidation from other diseases were randomly mixed with the CT scans of 11 patients with bronchioloalveolar carcinoma. Two independent observers who were unfamiliar with the cases classified 10 and nine of the 11 patients with bronchiololalveolar carcinoma, respectively, as positive for bronchioloalveolar carcinoma by applying the CT angiogram sign, and classified as negative 25 and 23 of the 26 patients without bronchioloalveolar carcinoma, respectively, for an overall specificity of 92.3%. The angiogram sign appeared on the CT scan because of the low-attenuating consolidation, which was caused by the production of mucin or other fluid and the intact bronchovascular framework within the tumor.

Index terms: Lung neoplasms, 60.1211

Radiology

Lung

#{149}

1990;

Bronchi, 60.3216 neoplasms, 176:749-753

neoplasms,

60.3216.

Lung neoplasms, CT, diagnosis, 60.3216

#{149}

‘ ‘

B

#{149} Eun #{149} Yup

on

Ju Yu, MD Yoon, MD

#{149} Joon

Koo Han, MD Doo Lee, MD

#{149} Jong

CT

RONCHIOLOALVEOLAR

the

carcinoma

Departments

neous lower attenuation of the consolidated lung as compared with that of muscle. To assess the specificity of those findings for bronchioloalveolan carcinoma, we used 26 cases of lobar consolidation caused by other diseases. These cases were randomized with the bronchioboalveolan carcinoma cases and tested. MATERIALS

those the the

nine

in

two;

and

requests

Address

to J.G.I., Department

nostic Radiology, Seoul Hospital, 28 Yongon-dong 110-744, Korea. C RSNA, 1990

Uni-

re-

of Diag-

National University Chongno-gu, Seoul

and

on

2-second

cab Systems)

lung

half

biopsy

bobectomy

in

scanning

time,

(4-second

scanning

mAs, 120 kVp). Scanning was after bolus injection of 100 mL mate meglummne sodium 66% tent, 30%) (Telebrix-30; Andre Aulnay-sous-Bois, France) and

of sodium two. Total

National

Fund.

than

200

mAs, 120 kVp in one). In the remaining patient, scans were obtained with a Delta Scan 2060 scanner (Technicare, GE Medi-

Hospital

Research

CT scans

of more

three. CT scans were obtained with a CT/T 9800 scanner (GE Medical Systems, Muwaukee) in 1 1 patients (3-second scanning time, 210 mAs, 120 kVp in eight; 4second scanning time, 400 mAs, 120 kVp

versity

24. Supported

Seoul

whose

on transbronchial

patients

by

April

with

area of a lobe or lobes, bounded by intenlobar fissure. Pathologic proof

April

the

of 43 patients bronchioboalveobar

consolidation

was based in

METHODS

from four instituover a period of 5 1989, we reviewed

of 12 patients

showed

in part

from

CT scans proved

carcinoma, collected tions and obtained years from 1984 to

ceived

17; accepted

AND

Among the pathologically

drip

grants

Mi Park, MD Soo Lee, MD

#{149} Kyung

of Radiology (J.G.I., M.C.H., E.J.Y., J.K.H., J.M.P., C.W.K.) and Pathology (J.W.S.), College of Medicine, Seoul National University, Korea; Department of Radiology, College of Medicine, Kyung Hee University, Seoul (Y.Y.); Department of Radiology, College of Medicine, Yonsei University. Seoul (J.D.L.); and Department of Radiology, College of Medicine, Soonchonhyang University, Chonan, Korea (K.S.L.). Received January 29, 1990; revision requested March 12; revision re-

print

From

#{149} Jeong

Carcinoma: Scans

is a peculiar type of lung cancer with mixed histologic features, confusing clinical manifestations, and varied radiographic manifestations (1-4). It is known to arise beyond a recognizable bronchus with a tendency to spread locally in the peniphenal air space, using the lung structunes as stroma without destroying underlying architecture (2,3). By nadiography, the consolidation type is known to account for 30% of all bronchioboalveolar carcinomas (5). When it appears as bobar consolidation, the primary clinical concern is pneumonia in most cases (6). Reports on the computed tomographic (CT) findings in bnonchioboalveolar carcinoma have dealt with the detectability of multiple lesions (7), bronchial changes in the loban form (8), peripheral lesions with pleural tags (9), and diagnostic cnitena in the solitary form (10). From a review of CT scans obtamed in patients with lobar bronchioloalveolan carcinoma after intravenous administration of contrast material, we observed these common findings: (a) branching pulmonary vessels extending more than 3 cm along a single channel (the CT angiogram sign) and (b) diffuse homoge-

I

Radiology

infusion

of

50 mL

time,

200

performed of ioxitala(iodine conGuerbet,

during

of contrast

the

medi-

um in eight patients with bnonchioboabveolar carcinoma and in all 26 patients with other diseases. Of the remaining four patients with bronchioboalveolar carcinoma, the contrast medium used was a bolus injection of 100 mL of sodium and meglumine ioxitabamate (iodine content, 38%)

and

(Telebnix-38;

continuous

Andre

drip

Guerbet)

infusion

and meglumine iodine content

in

ioxitalamate in all patients

ranged from 38 to 57 g. Contiguous scans with 1-cm collimation were obtained covering the entire thorax. Scans were photographed with

window

width

of 300-400

two

of 150 mL

in

a

HU and a level 749

b.

C.

Figure dyspnea.

1.

Bronchioboalveolar

(a) Chest

cell

radiograph

carcinoma;

shows

50-year-old

woman

areas of homogeneous

with

bronchorrhea

air-space

and

consolidation

in both

lungs with volume loss of the left lung. Several nodular areas of increased attenuation are also seen in right lower lobe. (b) Postcontrast CT scan at level of right upper lobe bronchus (window width, 400 HU; bevel, -20 HU) shows homogeneous consolidation of the right upper lobe. The consolidated lung shows diffuse bow attenuation (26.3 HU) compared with that of muscle (73.4 HU). Segmental bronchi are patent (white arrow) and run with opacified pulmonary artery (115.6 HU) (black arrow). Margin of the consolidated lung shows undulated border (arrowheads). (c) Scan 3 cm below b (window width, 350 HU; level, 0 HU) shows opacified, stretched pulmonary arterial branches emerging from the right interbobar pulmonary

artery

(curved

arrow)

low in attenuation. The heart fect by the volume-expanded tent bronchi within sure (arrowhead).

of 0 to -20 ments trast

scans

were

of seven

lung

(straight

postcon-

with

tients

bronchioboalveobar

distinguish-on

the

basis

pacarci-

to

CT an-

structive

pneumonia,

monia

three

carcinoma

caused

with

and

monary

with

case

mitral

population

independently.

cases were

reviewed,

of pulvalvular

troduction

session

criteria readers visually

Before

there explaining

the

test

was a brief

in-

the

pro-

with a model case (Fig 1). were asked whether they recognize

the

gram

sign and low-attenuating

tion.

For each

of these

two

CT angio-

consolidaitems,

they

were asked to rank their confidence of visual perception as 0 (not recognizable), 1 750

#{149} Radiology

is remarkably

left

mild

seen

bulging

but

Eleven

lung.

not

Note

ef-

also

pa-

of the major

definite),

fis-

2 (recog-

and definitely recsum of each score was 3 or more, the bronchioloalveolar

cases

veolar carcinoma, excluding case, and 26 cases of diseases carcinoma

the model other than were

ran-

domized. Microscopic

specimens gist

with

and/on

gross

pathologic

were

reviewed

by a pathobo-

special

reference

to the

inant

tumor

lion

of mucin

predom-

cell type and to the producor other

fluid.

The 12 patients with lobar bronchioboalveolar carcinoma consisted of nine women and three men. Their ages ranged from 36 to 76 years, with a mean of 57.8 years. All patients had a cough. Six patients (50%) had copious amounts of thin whitish sputum (bronchorrhea). At bronchoscopy, eight patients had excessive frothy secretion within the bobar bronchi. Consolidation involved entire lobes (Figs 1-3) in seven patients and a part but more than half of a lobe in five patients (Fig 4). Using

the

a.

of bronchioboab-

RESULTS

one case of

one

which

ob-

heart disease. To eliminate bias, those cases that showed a definite central mass or marked volume loss of the involved lobe were excluded. Two radiologists who were unfamiliar with the cases and blinded to the clinical information were asked to review the test

Both could

and

organism,

cases of actinomycosis,

pseudolymphoma,

posed

arrow)

of the

five cases of pneu-

by an unknown

infarction

loss

bronchioloalveolar

giogram sign-between bronchioboalveobar carcinoma and other diseases that cause lobar consolidation, a test population of 26 cases was compiled. The cases included eight cases of tuberculosis, eight cases of central lung cancer other than bronchioboalveolar

to volume

carcinoma.

ability

of the

lobe,

nizable), or 3 (clearly ognizable). When the (ranging from 0 to 6) case was regarded as

bron-

and seven

the test observer’s

middle

to the left side due to a compression

(probably

with

done

carcinoma

noma. To evaluate

and

vessels,

chioloalveolar without

lobe

lung,

patients

consolidated

middle

measure-

consolidated

and the muscle

the

displaced

the consolidated

HU. Attenuation

of the

within

is markedly

CT angiogram

sign

and

low-attenuating consolidation as indicators of bnonchioboabveolan carcinoma, the two observers correctly in-

tenpreted this disease in 10 of 1 1 and nine of the 1 1 cases, respectively. Among the 26 test cases without bronchioloalveobar carcinoma, the two observers made a false-positive diagnosis of bronchioloalveolar carcinoma in three and one cases, respectiveby, for an overall specificity of 92.3%. CT attenuation of the consolidated lung measured in seven patients with bronchioboalveolar carcinoma ranged from 8.7 to 53.1 HU, with a mean of 27.6 HU. Measured CT attenuation of the pulmonary vessels within the consolidated lung in three patients ranged from 104.7 to 150.9 HU, with a mean of 123.7 HU, and that of the muscle ranged from 69.7 to 77.5 HU, with a mean of 74.0 HU. The consolidated lung in patients without bronchioboalveolar carcinoma was generally of the same attenuation as muscle, obscuring the pubmonary vessels (Fig 5), and usually contained areas of heterogeneous attenuation. The only exceptional case, which was classified as bronchioboSeptember

1990

epithelium with evidence of mucin production in 10 patients. In the nemaining patients, predominant cell types were cuboidal cell and Clara cell (hobnail pattern), respectively, with evidence of fluid secretion of undetermined nature. The CT angiogram sign was more conspicuous in the former 10 patients than in the batten two patients. DISCUSSION

a. Figure

Bronchioloalveolar carcinoma is a distinct variant of adenocancinoma, composing up to 9% of all primary lung cancers (1 1,12). It charactenisticalby grows along the preexisting structure of the lung without destroying the underlying framework (lepidic growth) (2,3). Bronchioboalveolar carcinoma con-

b. 2.

weakness.

Bronchioboalveolar

(a) Chest

cell

radiograph

carcinoma;

shows

76-year-old

opacification

woman

of the right

with

lower

cough

lobe,

and

general

obliterating

the

right diaphragmatic dome. (b) CT scan shows consolidation of the right lower lobe. The attenuation of the consolidated lung (23.4 HU) is remarkably lower than that of muscle (77.5 HU). Note enhanced (104.7 HU) branching pulmonary vessels (arrows) within the lung. Anterior convexity of the right major fissure (arrowheads) suggests volume expansion of the right bower lobe due to mucin pooling.

a. Figure

b. 3.

Bronchioboalveolar

cell carcinoma;

42-year-old

woman

with

cough

and

bron-

chorrhea. (a) CT scan shows low-attenuating consolidation of the right lower and middle lobes. Note enhanced pulmonary vessel (straight arrow) and patent bronchi (curved arrow) within the lung. (b) Scan 6 cm below a shows bow-attenuating consolidation of the right bower lobe, which contains enhanced pulmonary vessels (arrows).

alveolar servers, farction vular

carcinoma was a case

by the two of pulmonary

with underlying heart disease and

mitral

obinval-

idiopathic thrombocytopenic purpuna (Fig 6). CT attenuation of the consolidated lung measured in seven patients without bronchioboalveoban carcinoma ranged from 62.0 to 92.9 HU, with a mean of 73.5 HU. Mean CT atVolume

176

#{149} Number

3

tenuation of the muscle was 71.5 HU (range, 62.5-81.9 HU). Round or oval areas of slightly high attenuation in the vicinity of the bronchi within the consolidated lung that were regarded as pulmonary vessels revealed a mean CT attenuation of 1 17.2 HU (range, 105.1-130.1 HU). Review of microscopic specimens showed predominantly tail columnar

sists

of mucus-filled

tall

columnar

cells that are most common and simibar to bronchial cells and cuboidal cells, which resemble type II pneumocytes. Other constituents are Clara cells (hobnail pattern) and ciliated cells (3,13). Mucus secretion is present in about 80% and may be extensive enough to produce mucoid pneumonia (3). Clinically, six of the 12 patients in our series had whitish and frothy bronchorrhea. At bronchoscopy, eight patients had excessive frothy secretion within the involved loban bronchi, and microscopically 10 patients had evidence of mucin secretion. Loban consolidation is an uncommon pattern produced by bnonchioboalveolan carcinoma that was initialby described by Mussen (14) in 1903. The gross lesion may involve a single lobe or an entire lung and may simulate boban pneumonia in the stage of gray hepatization (2,6). Whether lobar consolidation involves a single lobe or multiple lobes, the lesions are regarded as diffuse or advanced disease. Unlike the solitary nodular form, the prognosis in cases of the loban consolidating form is known to be poor regardless of therapy (6,15). Progressive radiographic and clinical deterioration was observed in our cases, as it was in the study of Epstein etal(6). Visualization of normally branching pulmonary vessels within the consolidated lung on postcontrast CT scans requires two factors. One is that the consolidated lung should have considerably lower attenuation than the enhancing vessels and the other is that distorted

ment

vascular trees significantly

by the

pathologic

should not in arrange-

process. Radiology

be

The #{149} 751

pneumonic form of bronchioboalveolan carcinoma fulfills these requirements by the production of mucin or another fluid substance flooding the alveolar spaces and by the growing characteristics of the tumor, defined as lepidic. Measured CT attenuation of the consolidated portion ranged from 8.7 to 53.1 HU, as compared with that of the muscle, ranging from 69.7 to 77.5 HU in our series. The mean difference in attenuation between the consolidated lung and the pulmonary vessels within the consolidated lung in patients with bronchioboalveolar carcinoma was 96.1 HU, while that in patients without bronchioloalveolar carcinoma was 38.7

HU.

Technical

factors

that

affect

the visibility of pulmonary vessels on a CT scan include the amount of iodine administered, the rate of contrast material administration, the timing of the scan, and the width of the CT window. Mucin pooling seems to be exaggenated in lobar bronchioloalveolar carcinoma, due probably to the sealoff effect of the interlobar fissure. This assumption is supported by the higher prevalence of clinical bronchonnhea: five of eight patients with bobar bronchioboalveolar carcinoma in the study of Epstein et al (6) and six of 12 in our series had clinical bronchonrhea, compared with 5%27%

(1,16-18)

in overall

of pulmonary

venous

return

by

a left atnial thrombus probably enforced intnaalveolan fluid collection, resulting in lower-attenuating consolidation. CT scans of patients with pneumonic consolidation-caused by ordinary bacteria, tuberculosis, or fungal infection-that were compared with scans of patients with bnonchioloalveolar carcinoma in our series showed nonuniform enhancement of 752

.

Radiology

b. cell

carcinoma;

61-year-old

woman

border of masslike consolidation opacified pulmonary vessel (arrows) within the low-attenuating (b) Photograph of gross cut section from the resected left lower pulmonary artery (straight arrows) and accompanying bronchus tumor

mucin

mass (arrowheads). Microscopic vacuole and intraalveolar mucin

section showed substance.

typical

with

productive

cough.

in the left lower lobe. Note portion of the tumor. lobe shows intact branching (curved arrow) within the tall

columnar

epithelium

with

bronchio-

loalveolan carcinoma. The bulging of the interlobar fissure shown in our cases (Figs 1, 2) is a radiobogic support of that assumption. In cases of the solitary nodular form of bronchioloalveolan cancinoma, visualization of enhanced pulmonary vessels within the nodule would be difficult, because the tumor encompasses only a short segment of the vessels and possibly because the tumor produces bess mucous fluid than do tumors in the lobar form. Pulmonary edema caused by increased hydrostatic pressure or a pulmonary infarction in the acute stage may produce the angiogram sign on a CT scan, as shown by a patient in our test population (Fig 6). Obstruction

a. Figure 4. Bronchioloalveolar (a) CT scan shows undulating

5.

Figures

6.

5, 6.

(5) Tuberculous

pneumonia.

CT scan

shows

patent

bronchi

with

somewhat

stretched appearance and undulated border. The attenuation of the consolidated lung is slightly higher (71.8 HU) than that of the muscle (62.5 HU), preventing visualization of the pulmonary vessels. Measured attenuation of the aorta was 109.6 HU. (6) Pulmonary infanction; 45-year-old man with underlying mitral valvubar heart disease and idiopathic thrombocytopenic purpura in whom the false-positive diagnosis of bronchioboalveobar carcinoma

was made when the right middle thrombus

within

the angiogram sign was applied. Note lobe and faintly opacified pulmonary the

enlarged

left

atrium

is seen

the consolidated lung and usually showed localized areas of focal low attenuation. In cases of postobstructive pneumonia caused by lung cancen, the attenuation of the consolidated lung was generally the same as or slightly higher than that of the muscle. The main reason for the absence of the CT angiogram sign in those patients without bronchioboalveolan carcinoma is the smaller difference in attenuation

(43.7

HU)

between

the

consolidated lung (73.5 HU) and the pulmonary vessels (1 17.2 HU). Epidermoid carcinoma with central bronchial obstruction and distal post-

the low-attenuating artery (arrowheads).

consolidation Intraatnial

of

(arrows).

obstructive

drowned

lung

could

show the angiognam sign on a CT scan. However, the presence of a central bronchial obstruction and mass would be helpful findings in differentiating epidermoid carcinoma from bobar bronchioloalveolar carcinoma. Postobstructive endogenous or exogenous lipid pneumonia theoretically could show enhanced pulmonary vessels, due to relatively bow attenuation of the consolidated lung. However, neither of the two patients with pathologically

proved

tive lipid pneumonia showed the angiognam

postobstruc-

in our sign

series at CT.

September

1990

In conclusion, our study shows that the CT angiogram sign appears commonly in patients with lobar bronchioboalveolar carcinoma and is highly specific for bronchioboabveobar carcinoma. However, the apparent value of this sign now needs to be confirmed in a larger, prospective study. U

5.

6.

7.

8.

Hill

3.

Liebow

4.

Knudtson KP, Lawrence BJ. (“alveolar cell”) carcinoma J Thorac Surg 1953; 26:331-406.

AA.

Adv

Bronchiolo-alveolar

Intern

Thunlbeck New

Med

WM. York:

Miller

13.

Lo-

Husted

GG.

ma: two clinical logic diagnosis.

of

I,

the

lung.

345-346.

Freiman

Bronchioloalveolar

carcino-

entities with one pathoAJR 1978; 130:905-912.

two

176

#{149} Number

3

hundred

A. cell

Terminal cancer

sixty-five

cases.

bron-

of the

lung:

Cancer

1966;

Assist

16.

lan-cell carcinoma of the lung. Radiology 1969; 92:793-798. Ludington LG, Verska JJ, Howard 1, Ky-

Im

Tomogr

CB

1981;

Jr. Anger

PH,

5:830-833.

J-G,

Choi

BI,

of

lobar

bronchioloalveolar

Steinbacher

Park

JH,

Assist

et al.

CT

find-

noma

1986; 10:320-

tor:

M, van HH.

Kaick

radiological

findings

lung.

Kuhlman

JE,

G, Schaaf

Computed

Fishman

J,

17.

tomographic in alveolar

ROFO

cell

18. EK,

Kuhajda

1988;

FP,

et

carcino167:379-

The

G, Brewer

(alveolar a review

61:622-628. Marcq M, cinoma: natural

1985;

Primary carcinoma of the Pa Bull 1903; 16:289-296.

YM.

pnidakis

carcino-

Tomogr

carcinoma of the 142:267-269.

many

LA.

cell),

Galy

P.

of alveo-

Bronchiolar

another

of 41 cases.

clinicopathologic history, and

facets

Chest

carci-

great 1972;

Bronchioloalveolar

car-

relationships, prognosis in 29 cases.

Am Rev Respir Dis 1973; 107:621-629. McNamara JJ, Kingsley WB, Paulson Arndt JH, Salinaslzaquirre 5, Urschel Alveolar cell (bronchiolar) carcinoma the

lung.

J Thorac

imita-

Cardiovasc

Surg

DJ, HC. of

1969;

57:648-656.

Edgerton R, Rao U, Takita H, Vincent RG. Bronchioloalveolar carcinoma: a clinical overview

12.

Farpour

19:776-780.

382.

11.

or alveolar

Berkmen

Mulhern

al. Solitary bronchioloalveolar ma: CT criteria. Radiology

D, Atkinson

WL,

chiolar

15.

and

10.

Watson

Coleman BG, Epstein DM, Gefter WB. CT differentiation of solitary from diffuse bronchioloalveolar carcinoma. J Comput

Vollhaber

10:329-358.

Pathology 1988;

9. of

carcino-

1960;

Thieme,

WT,

B, Pietra

Volume

a

322.

Storey CF. Bronchiolar the lung. ma.

carcinoma:

Musser JH. lung. Univ

RA,

ma. J Comput

References

2.

Bronchioloalveolar

14.

Metzger

ings

1.

CA.

review. Radiology 1984; 150:15-20. Epstein DM, Gefter WB, Miller WT. bar bronchioboalveolar cell carcinoma. AJR 1982; 139:463-468.

and

bibliography.

Oncology

1981; 38:269-273. Edward CW. Alveolar carcinoma: view. Thorax 1984; 39:166-174.

a re-

Radiology

#{149} 753