Gordon Stephen
L. Weisbrod,
J.
MD, FRCPC MD, FRCPC
Herman,
Thin-walled
Mark Frederick
#{149}
J. Towers,
MB, FRCR #{149} Dean W. Chamberlain, R. K. Matzinger, MD, FRCPC
#{149}
Cystic
cystic
lesions
study, were
Carcinoma’
thin-walled
identified
dation
should
include
B
(BAC)
of thin-walled with consoli-
ferent
terms:
Lung
neoplasms,
Radiology
Lung,
1992;
cysts,
60.3129,
60.3216
60.3216 185:401-405
many
are
those
lobar
atelectasis,
and
in preexisting
Cavitation,
although
cysts
uncom-
mon, may occur in single and multiple lesions (2). Isolated cases of multiple cavitary lesions in BAC have been reported (9-19). We describe four patients with proved BAC showing thinwalled cystic lesions.
CASE 1.-A
Patient
REPORTS
49-year-old
woman
with
chronic asthma developed a nonproductive cough, sore throat, and malaise over 4 weeks. Posteroanterior (PA) chest mild
radiography
showed
posterior
and
segment
in both
cystic
per
consolidation
lower
lesions
lobe
right
Multiple
present
(Fig la).
left upper size from
of the
were
(CT) showed
thick.
upper left
nodules
nodules and had cysts
in the
varied in walls only
had
thicker
walls, and some solid nodules also present (Fig ib). A chest radiograph
tamed
2 years
earlier
parenchyma
Open showed along
tent
with
BAC.
throughout was From the M.J.T., S.J.H.)
of Radiology (G.L.W., (D.W.C.), Toronto Hospital, 200 Elizabeth St. Toronto, Ont, Canada M5G 2C4, and the Department of Radiology, Ottawa Civic Hospital, Ottawa (F.R.K.M.). Received February 14, 1992; revision requested March 31; revision received April 29; accepted May 13. Address reprint requests to G.L.W. C RSNA, 1992 I
Departments and Pathology
cystic
Foci
the
evident.
walls,
copy
confirmation
allowed
A follow-up later showed
cystic
lower lesions
but
CT
seen
micros-
of the
diagno-
type). obtained of the
scans
of lung
piratory
infections
had
a known
cyst
in the right
woman
for many
thin-walled
congenital, radiography
admission, showed
PA a large,
levels tion around
cough. res-
years
and
mu!ti!ocu!ated
lung.
sumed at chest
pre-
unproductive for intermittent
The
cyst
was
pre-
having been identified 3 years previously. chest radiography thin-walled cyst
At
(Fig with
2a) air-
in the right lung. Consolidathe cyst was mainly in the
right lower lobe. Multiple, small ill-defined nodules were present in the middle and
upper
portions
some
contained
The
left lung
of the
right
central
was
lung,
areas
normal.
firmation
of a multilocular
rounding
consolidation
and
of blackness.
CT allowed cyst
with
in the
right
Multiple, small thin-walled cystic 5-15 mm in diameter were present right lung, especially in the upper (Fig 2b, 2c). Bronchoscopy biopsy of the
inflammatory with
CT repeated crease
the right ules
and
lung,
in the
was
later
and
increasing
the cyst. from the
mucus-producing cm in diameter
were
dIe lobe, and cavities measured largest genic
of these (Fig
right
upper
middle and multifo-
BAC. Cavities up to found in the mid-
in the lower
appeared 2d),
nodcon-
lobe
up to 9 cm in diameter. cyst
in
of small
lobe and resection of the right lower lobes showed widespread cal 2.5
in-
of nodules
development
around biopsy
only.
ineffective.
showed
number
left lung,
solidation A wedge
change
antibiotics
8 weeks
in size
lung. nodules in the lobe
and percutaneous needle lower lobe consolida-
right
revealed
tion
Treatment
consur-
while
to be most
The a bronchoof the
others
thought to have been due to postobstructive bronchiectasis. These were colonized to various degrees by secondary tumor
growth
appeared tumor
(Fig
to have necrosis
Follow-up months gression
(Fig
chest
after surgery of disease
2e).
formed
A few
smaller
secondary
cysts
to
20.
radiography
and
CT 7
showed marked proin both lungs. At CT,
1 year lesions.
through
demonstrated
in areas
not
Electron
CT scan progression
lobe
present
no necrosis
were
(mucus-secreting
High-resolution
right
were
lesions
material.
extend-
is consis-
of tumor
in the biopsy sis of BAC
cells
(Fig
were
lobe
which
specimen,
Cystic
lung
disease.
epithelial
alveolar
were ob-
normal
of the left upper
malignant
ing
showed
without
biopsy
up-
tomography
cystic
Some
lobe
small
in the
Computed
small
lobe; these 6 to 15 mm
1-2-mm
in the
lobes.
CT scan
28-year-old
sented with a severe She had been treated
fluid
tumor
lung
on the previous
2.-A
Patient
The
of a solitary
peripheral pulmonary nodule, multiple nodules, and lobar or diffuse conso!idation (1-6). Unusual radiographic appearances include diffuse disease with minima! or no radiographic signs, expansile pulmonary consolidation without air bronchograms,
normal
Ic, Id).
dif-
appearances.
common
developing
BAC.
produce
radiographic
most
(7,8). Index
can
been
carcinoma
RONCHIOALVEOLAR
in four
patients with proved bronchioalveolar carcinoma (BAC). The radiographic appearances are described, and possible mechanisms of formation of the lesions are discussed. Although such appearances due to BAC have rarely been described in the literature, the authors believe that the differential diagnosis cystic lesions associated
FRCPC
Lesions
in Bronchioalveolar In a retrospective
MD,
the
thin-walled that
had
Abbreviations: noma, PA
=
BAC = bronchioalveolar posteroanterior.
carci-
diAl
a.
b.
Figure
1. Patient
left upper
1.
(a) PA radiograph
lobe shows
multiple
C.
of the
small
cystic
lesions in an area of consolidation. (b) CT scans show thin-walled cystic nodules, solid nodules, and consolidation in the right lung. (c) CT scan obtained 1 year !ater and (d) high-resolution CT scans show further development of thin-walled cystic lesions in
the right
small,
lower
lobe.
thin-walled
cystic
lesions
found to have developed in areas of previous normal
Patient man had
3.-A 57-year-old a diffuse reticu!ar
ley B lines,
small
suspected
lung
asymptomatic
infiltrate,
scattered
thin-walled
were
in the right parenchyma.
Ker-
nodules,
cysts
on
and
PA
and
d.
lateral chest radiographs. Two years earher, he had undergone gastrectomy and abdominal irradiation for a small, welldifferentiated !ymphocytic lymphoma !o-
calized
to the stomach,
ment
of other Whole lung
with
no
sites. tomography
DISCUSSION
its
involve-
BAC
is defined
as a generally
well-
was confirmed from open biopsy specimens of the right upper lobe. Bone metas-
differentiated peripheral primary lung adenocarcinoma, arising beyond a grossly recognizable bronchus, with a tendency to spread on the walls of the distal air spaces, which serve as the stroma for the neoplastic cells but are not scarred as a result of the tu-
tases
mor
I-cm-diameter
showed
thin-walled
small,
cystic
nodu!es
bilaterally (Fig 3). Percutaneous fine-needle aspiration biopsy was positive for malignant
cells,
consistent
developed
therapy, was not
with
rapidly
and the patient performed.
Patient
4.-An
p!ained malaise
BAC.
despite
chemo-
died.
Autopsy
82-year-old
woman
consolidation
in the
lung.
No improvement
with
seen.
Sputum
right
com-
lower
antibiotics
cytology
was
suspicious
for adenocarcinoma, and transbronchia! biopsy revealed adenocarcinoma spreading along the alveolar walls, which is consistent graphs
with BAC. Follow-up obtained 7 months
progression
of disease,
chest radiolater showed
with
involvement
of the previously normal left lung. Multipie, small, thin-walled cystic lesions with intervening
consolidation
cysts
had
died
of respiratory
ter.
Autopsy
402
#{149}
developed was
Radiology
not
between (Fig
4). The
failure
shortly
performed.
(20).
The
presence
adenocarcinoma
of a nonproductive cough and for I month. PA chest radiography
showed was
BAC
the patient
thereaf-
incidence
is said
Smoking
of a primary
elsewhere
the
in the
cell of origin
has been resolved by the electron microscopic findings that BAC represents a heterogeneous group of tumors that may arise from type II pneumocytes, nonciliated bronchiolar
(Clara) cells, or mucus-producing bronchiolar cells, or perhaps bronchiolar
entiation BAC primary
stem
into any represents pulmonary
cell
capable
from
In
contrast
neoplasms,
the
women
with
commonly monary
a
of differ-
of these (2,4,15,21). 1.S%-6.S% of all neoplasms, and
primary of BAC
cancer
form
lung in
is high in those
of disease
commonly
of pul-
appears
as a single
with
(6). BAC
develops in areas fibrosis (4,21,22).
most
(6).
associated
particularly
the localized
BAC
be rising
to other incidence
lung
(30%-5O%),
diographically
body precludes the diagnosis, because metastatic spread can produce an identical histologic appearance. The issue of unifocal versus multifoca! ori-
gin is not settled. Controversy about
(21).
to
is not strongly
ra-
pulmonary
nodule, multiple nodules, or single or multiple areas of consolidation (1-6). The solitary nodule form is slow growing, and mediastina! adenopathy and recurrence following removal are unusual, resulting in an excellent prognosis. In contrast, the diffuse form of the disease is relentlessly progressive,
and
vivors,
there
are
regardless
Atypical
few
long-term
of intervention
radiographic
sur-
(6,23).
appearances
of BAC include lobar atelectasis, expansile consolidation without air bronchograms, elongated lobulated opacity
and graphs
resembling
apparent with
on CT scans
mucoid
normal diffuse
chest disease
or at surgery
impaction,
radioevident
(7). November
1992
a.
d. Figure around
2. Patient the cyst
2.
(a) PA chest
in the
right
lower
b.
C.
e.
f.
radiograph shows a large, thin-walled cyst with air-fluid levels in the right lung. Consolidation lobe. Multiple, small, ill-defined nodules are present in the middle and upper portions of the
some contain central areas of decreased opacity (arrowhead). (c) a thin-walled mu!ti!oculated cyst with surrounding nodules, eosin stain; original magnifications, by malignant epithelium (curved lined by malignant epithe!ium.
x63) arrow), (1) Necrosis
show mechanisms and residual benign in a tumor nodule
Cavitation
in BAC is unusual because of the relative lack of necrosis (22) and the tendency of the tumor to preserve normal lung architecture (1 5). Cavitation occurred in 7.4% of patients (10 of 136 and nine (2,15,21,24),
of 122
patients)
in two
large
series
(1,25). Of 100 cavitary bronchogenic carcinomas reported by Chaudhuri, three were alveolar carcinomas (26). Cavitation in BAC may occur in single or multiple lesions (2). The wall thickness of the cavitary lesion is usually thick but may be thin (24,27). Intracavitary
BAC
is rare
aspergilloma
A radiographic tation can occur in several
appearance in association ways.
Preexisting
(28).
of caviwith lung
cysts
such
2d) (7,8), bronchiectasis), interstitial
(b, c) At CT, (b) thin-walled one showing of cavity formation ciliated epithelial (arrow).
cystic and solid nodules in the right upper lobe and cavitation, are evident. (d-f) Photomicrographs (hematoxy!inassociated with BAC. (d) A bronchogenic cyst is partially lined lining is indicated (straight arrows). (e) A bronchiectatic airway
as bronchogenic postinflammatory
cysts
(Fig
ular
cysts
(ie,
(4,5).
“honeycombing” fibrosis and healed
in granu-
lomatous disease, postinfarction cysts, and emphysematous bullae may antedate the development of malignancy
(29) and
may
be secondarily
cob-
nized by tumor growth. Their role (if any) in tumor pathogenesis is controversial. A radiographic appearance in which small areas of blackness within the lesion suggest cavitation can occur. These represent areas of focal emphysema
is present right iung
secondary
tion (29) or areas rendered airless,
to scar
retrac-
of normal lung not because of the irreg-
lepidic growth of the neoplasm Kuhlman et al (30) described
findings
of pseudocavitation
of solitary small,
oval
mimicking
BAC
in which
multiple,
areas
of low
attenuation
tiny
cavities
CT
in cases
were
seen
within or surrounding the periphery of the mass. The CT appearance of pseudocavitation may reflect the same process that gives rise to the air bronchogram
on
plain
radiographs:
the propensity of the tumor to proliferate along the walls of the alveolus without disrupting the overall lung architecture and with preservation of bronchiolar patency (29). Zwirewich et al (31) described bubblelike areas of air attenuation in 25% of malignant
nodules, type,
most
commonly
of the
at high-resolution
CT.
BAC
At patho-
logic evaluation, these corresponded either to patent small bronchi within the nodule or cystic spaces within papillary regions of tumor growth. True cavitation may occur secondary to tumor growth through ischemic necrosis (Fig 20. Necrosis within larger tumor nodules is usually ascribed to outgrowth of the blood supply to the center of the lesion, but this is unusual because the unique nondestructive growth pattern of BAC usually preserves perfusion to the involved area of lung. Diffuse BAC with multiple bilateral cavities has rarely been described (919). Interestingly, reports of this disease The
have lesions
mostly can
both
tomography
scans
of right
and
left
upper
lobes
show
small
come from Japan. be small, and the
walls can be remarkably thin (2,12,15). Ohba et a! (12) reported a 47-year-old woman in whom chest radiography showed bilateral, diffuse reticulonodular infiltrates with multiple cysts 3-10 mm in diameter and numerous small nodules with central pinholes. At autopsy, there was bilateral cystic destruction of the pulmonary parenchyma. The cystic spaces had two patterns: (a) carcinomatous cavities and (b) emphysematous cysts with less carcinoma in the wall. The pathogenesis of cyst formation was considered to be due to two main mechanisms: central necrosis within the nodule and, more commonly, check-valve obstruction at the terminal bronchiobar level. Thickened fibrous terminal bronchioles were found in some sections, which could account for the check-valve obstruction and formation of emphysematous cysts. Imai et a! (ii) reported a 70-yearold man who died of diffuse BAC. At autopsy,
Figure 3. Patient 3. Conventional thin-walled cystic nodules.
lungs
were
filled
with
Figure 4. Patient ing consolidation.
4.
PA
chest
radiograph
shows
diffuse
bilateral
cystic
lesions
with
interven-
disseminated whitish tumors accompanied by multiple cysts. Microscopically,
the
cysts
resembled
centrilobu-
bar emphysema. Histologically, the cysts were due to distended alveoli filled with abundant mucus. The walls were composed of BAC. Bronchiectasis was found in some areas. The authors suggested that tumor cells
extending
along
the
alveolar
walls destroyed the alveoli centribobu!ar emphysematous No
radiographs
The patient sions opsy.
were
cause of the 1 is uncertain
to form cysts.
shown.
cystic lesions in because the be-
were not revealed at lung biWe can only speculate that the
thicker-walled cystic nodules and the cysts arising in consolidated lung were due to ischemic necrosis resulting from tumor growth. The thinAn.,
walled cysts in the left upper lobe and those that subsequently developed in the right bower lobe were not present on previous chest radiographs or CT scans
and
could
be
due
to check-valve
terminal bronchiolar obstruction as proposed by Ohba et a! (12) or possibly cystic spaces within papillary regions
of tumor
growth.
The
barge
multibocubar cyst in patient 2 predated the BAC by at beast 3 years and likely represented a congenital bronchogenic cyst secondarily colonized by tumor growth (Fig 2d). The smaller cystic lesions presumably arose secondary to tumor growth through ischemic necrosis (Fig 20 and postobstructive bronchiectasis (Fig 2e). It is possible that air-containing cystic
spaces within papillary regions of the tumor contributed to the appearance. The lung biopsy in patient 3 did not reveal cavitary lesions, so their pathogenesis can therefore only be presumed to be similar to that of the besions in patient 1. Similarly, the cause of the cavitary lesions in patient 4 remains unproved. The differential diagnosis of multiple thin-walled cystic lesions in the lung includes congenitab causes (cystic adenornatoid malformation, bronchogenic cysts), airway diseases (bronchiectasis, bulbous emphysema), infections (tubercubous, fungab, hydatid cysts, pneumatocebes), emboli (septic, nonseptic), neoplasms (metastases, lymphoma, baryngeal
papillomatosis),
autoimmune
November
1992
diseases
(Wegener
9.
granulomatosis,
uborna),
causes nia)
trauma,
(congenital (32).
With
and
gran-
miscellaneous
diaphragmatic thin-walled
10.
her-
cystic
le-
sions, particularly if associated with consolidation, BAC should be a diagnostic consideration. U
11.
12. Acknowledgment: for her assistance manuscript.
We thank Rose in the preparation
Baldwin of this
13.
References 1. 2.
3.
Hill CA. Bronchioloa!veo!ar carcinoma: a review. Radiology 1984; 150:15-20. Berkmen YM. The many faces of bronchiolo-alveolar carcinoma. Semin Roentgeno! 1977; 12:207-214. Marzano MJ, Deschler T, Mintzer PA. Alveo!ar cell carcinoma. Chest 1984; 86:123-
14.
15.
128. 4.
5.
6.
7.
8.
Lafuente Perez
rheumatoid nodules), idiopathic causes (sarcoidosis, eosinophilic
Donaldson JC, Kaminsky DB, Elliot RC. Bronchio!ar carcinoma. Cancer 1978; 41: 250-258. Kittredge RD, Sherman RS. Roentgen findings in terminal bronchio!ar carcinoma. AJR 1962; 87:875-883. Epstein DM. Bronchioloa!veo!ar cardnoma. Semin Roentgenol 1990; 25:105-111. Huang D, Weisbrod CL, Chamberlain DW. Unusual radiologic presentations of bronchioloalveolar carcinoma. J Can Assoc Radiol 1986; 37:94-99. Prichard MG, Brown PJE, Sterrett CF. Bronchioloalveolar cardnoma arising in longstanding lung cysts. Thorax 1984; 39: 545-549.
16. 17.
18.
19.
20.
Diaz
J, lzquierdo F, Gallar P. Simo G, M, Camunez YF. Nodulos multiples cavitados. Rev Clin
pulmonares Esp 1988; 182:283-285. Nakano T, Tamura S. Hada T, Higashino K. Bilateral multiple cavities in bronchiolar carcinoma. Thorax 1988; 43:412-413. Imai 5, Sekigawa 5, Yamamoto H, et al. Bronchiolo-alveo!ar adenocarcinoma with multiple cysts. Acta PatholJpn 1982; 32:
21. 22. 23.
24.
Edwards CW. Alveolar carcinoma: a review. Thorax 1984; 39:166-174. Liebow AA. Bronchiolo-alveolar cardnoma. Adv Intern Med 1%0; 10:329-358. Miller w-r, Husted J, Freiman D, Atkinson B, Pietra GG. Bronchioloalveolar carcinoma: two clinical entities with one pathologic diagnosis. AJR 1978; 130:905-912. DeJong PM, Busscher DLT, Bakker W. Bronchio!oa!veolar cardnoma presenting
677-682.
as a thin walled
Ohba 5, Takashima T, Hamada 5, Kitagawa M. Multiple cystic cavitary alveo!ar-cell carcinoma. Radiology 1972; 104:65-66. Seibel MJ, Witzleben Ev, Lesch R. Bilatera! cavitary bronchiolo-alveolar carcinoma of the diffuse type. Prax KIm Pneumol 1987; 41:49-52. [German] Mon Y, Mon M, Koba M, Yamagishi M, Suzuki A. CT findings of bronchiolo-alveolar carcinoma with special reference to the lucencies within abnormal shadows (abstr). Jpn J Clin Radio! 1989; 34:85-90. Scully RE, Mark EJ, McNeely WF, McNee!y BU. Weekly cinicopathological exercises. N Eng!J Med 1989; 321:375-385. Wormer DC. Cavitary bronchiolar cardnoma. Am Rev Respir EMs 1969; 99:773-776. Bovornkitti 5, Limsila T, Prabhasawasdi D, Stitnimankarn T. Multiple cystic pulmonary alveolar cell cardnoma. J Med Assoc Thai 1970; 53:739-745. Seki Y, Fukuma 5, Sawada K, et a!. Bronchiolo-a!veo!ar cell cardnoma: report of an autopsy case with a 21-year clinical history followed by chest x-ray examination. J Jpn Lung Cancer Soc 1980; 20:59-64. [Japanese] Higashiguchi R, Katada H, Ueno M, et al. A case of bronchiolo-alveolar type papillary adenocarcinoma presenting with multiple cavities. JJpn Lung Cancer Soc 1984; 24:743-748. [Japanese] Carter D, Eggleston JC. Tumors of the lower respiratory tract. Fascicle 17, second series. Atlas of Tumor Pathology. Washington: Armed Forces Institute of Pathology,
Thorax Greco
1980.
25.
Surg 26.
28.
29.
30.
31.
32.
man.
1986;
41:652-656.
Chaudhuri
tating 27.
cavity in a young
1989; 44:230-231. RJ, Steiner RM, Goldman 5, Cotler H, Patchefsky A, Cohn HE. Bronchoalveolar cell cardnoma of the lung. Ann Thorac MR. Primary pulmonary cavicardnomas. Thorax 1973; 28:354-366. CJ, Hooper RG, Beech!er CR. Thincavitary bronchio!ar cardnoma.
Tellis walled Chest 1977; 71:239. Mays EE, Hawkins JA. Cavitary bronchio!ar cardnoma with intracavitary aspergilloma. Am Rev Respir Dis 1967; 95: 1056-1060. Shapiro R, Wilson CL, Yesner R, Shuman H. A useful roentgen sign in the diagnosis of localized bronchioloalveolar cardnoma. AJR 1972; 114:516-524. Kuhlman JE, Fishman EK, Kuhajda FP, et a!. Solitary bronchioloa!veo!ar carcinoma: CT criteria. Radiology 1988; 167:379-382. Zwirewich CV, Veda! S, Miller RR, Muller NL. Solitary pulmonary nodule: highresolution CT and radiologic-pathologic correlation. Radiology 1991; 179:469-476. Godwin JD, Webb WR, Savola CJ, Gamsu C, Goodman PC. Multiple, thin-walled cystic lesions of the lung. AJR 1980; 135:
593-604.