DEEMBER, I(68

RADIOLOGY AN1) HONEYCOMB LUNG 1)ISEASE*

B’ ‘F. H. JOHNSON, JR., Ml).
MEMPHIS, 1 ENNESSEE
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T HE recognition and diagnosis of the

multiple causes of honecomb lung
disease are complicated by the inaccurate
definitions of terms. The original usage #{149}
4#{149} -
was a gross patholog term employed at
11
autops\’ to (lescribe lungs with a worm-
eaten or honeycomb appearance.” The
involvement could be lobar or generalized.
The roen tgenograph ic recogni tion of
honeycomb lung disease implies the ViSU-
alization of multiple lucent shadows from
2 mm. to 10 mm. in size (Fig. i). We often
use the term in reference to a disordered
multicvstic visualization, regardless of size,
that appears similar to a wasp nest thrown
down and trampled. This disordered multi-
lucent visualization is frequently seen as
disease but rarely follows a predictable
pattern of development or involvement.
The lungs are made up of vessels, lym-
phatics, a small amount of interstitial tissue,
and a large amount of air (inside bronchi,
11G. i. A honeycomb, lower left, is only one type of
alveolar spaces, etc.). Pathologic involve- reticular (net-like) pattern. Other examples il-
ment of the differential densities of these lustrated reveal the order or disorder of various
few structures produces a tremendous reticular patterns.
number of variations in the roentgeno-
graphic visualization of diseases. On the changes of disseminated interstitial pul-
other hand, several diseases may present a monary diseases.
similar roentgenographic appearance; in The statement is often made without
which case a differential diagnosis is neces- specific documentation that a honeycomb
sar-. A roentgenographic hone\comb ap- pulmonary pattern is the only reliable sign
pearance requires a sophisticated differen- of interstitial lung disease. This does not
tial diagnosis and factual integration for mean, however, that all roentgenographic
accurate interpretation. honeycomb patterns are conclusively inter-
Optical perception plas a significant stitial disease, as would be the case with a
part in the diagnosis of honeycomb lung gross pathology honeycomb appearance.
disease.’’ Multiple scattered miliary nod- A review of the literature and our personal
tiles in appropriate groupings are resolved experience reveal confusion regarding a
by the eye as apoorly-outlined honeycomb good differential diagnosis of the roentgeno-
appearance, as are multiple longer strands logic entity, “honeycomb lung disease.”
of disordered arrangement (Fig. 2, A-F). This confusion has evolved into the follow-
Felson’ has previously demonstrated the ing approach:
thickened septal walls and edematous wall A chest roentgenogram with a honey-

* From the Department of Radiology, The University of Tennessee College of Medicine, Memphis, Tennessee.

8io
 \o. 104, No. Radiology and Hone’comb Lung Disease I I
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-- ‘0’’:,.. #{149}:Q;.f. ;,:‘#{149}“i..#{149}..

“-4” .

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.-

11G. 2. The photographs of millet seeds and sunflower

(A, C and E) are compared seeds to their roentgeno-
grams (B, D and F). When the composition millet (A), the roentgenogram
is entirely (B) reveals an
orderly granular pattern. A mixture of millet and sunflower seeds (C) produces the roentgen appearance of a
honeycomb pattern (D). Sunflower seeds alone (E) also produce a honeycomb pattern (F), but the pattern
is more disordered and strandlike as in fibrotic pulmonary diseases.

comb pattern is first evaluated for a pre- the natural history of interstitial diseases
dominant miliary or strandlike appear- and may either progress to fibrotic strand-
ance. The miliary pattern appears early in ing or disappear. Most diseases with a vascu-
 812 T. H. Johnson, Jr. DECEMBER, 1968

litis reaction or hematogeneous basis seem TABLE I (Continued)

to visualize as a fusion of miliary dots.
Co!!agen Diseases
Sporadic multiple respiratory acinous opac-
Scieroderma
ification produces a similar appearance.7 Periarteritis nodosa
The sparse strandlike patterns of fibrotic Lupus erythematosus (less frequently)
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scars and interstitial thickenings resolve I)ermatomyositis

optically as a sharp focus honeycomb pat- Rheumatoid disease of lung

tern in contradistinction to the softer

Ma!ignant Diseases
granularity of the miliary honeycomb
Lymphangitic spread
(Fig. 2, A-F). Leukemic infiltrates
A second point of evaluation is the Lymphoma with spread
character and timing of changes in the pat-
tern. Probably the most important factor Rare Causes

of evaluation is clinical symptomatology. Tuberous sclerosis (muscular cirrhosis of lung)

Myomatosis (“von Recklinghausen’s”)
If the roentgen diagnosis does not agree
Leiomyomatosis of lung
with the clinical findings, we must review Adenomatosis of lung
the possibilities of another diagnosis, and Giant cell pneumonia
the proper diagnosis must be assumed. Hamman-Rich syndrome

Table i shows the results of reviewed and

Storage Diseases
Histiocytoses (histiocytosis X)
TABLE I
Eosinophilic granuloma
DEFINITE CAUSES OF HONEYCOMB LUNG Hand-Sch#{252}ller-Christian disease (cholesterol
histiocytosis)
Common Causes Letterer-Siwe’s disease (non_lipid histiocytosis)
Niemann-Pick’s disease
Saccular
Gaucher’s disease
Bronchiectasis
Bronchiolectasis
Bullous emphysema of lung
Diffuse interstitial fibrosis of lung experienced causes of roentgenologic honey-
comb lung disease. These causes lend them-
Acute Infections
selves to the somewhat artificial separation
Influenza
Herpes zoster (chicken pox)
listed, and each category will be illustrated
Tuberculous bronchopneumonia (galloping con- and discussed individually. After listing
sumption) the definite causes of a honeycomb picture,
there are several possible causes (Table ii)
Chronic Diseases which cannot be completely excluded from
Chronic lipoid pneumonia
Pneumoconioses
Silicosis TABLE H
Asbestosis
POSSIBLE CAUSES OF HONEYCOMB LUNG
Berylliosis
Bauxite pneumoconiosis
Other reactive dusts Desquamative interstitial pneumonia
Farmer’s lung

Granu!omatous Diseases Inhalation of hot mercury fumes

Streptomycin treated tuberculous
Chronic tuberculosis
bronchopneumonia
Fungus diseases (chronic)
Idiopathic pulmonary hemosiderosis
Sarcoidosis
(terminal stages)
Wegener’s granulomatosis
Chronic mitral valve disease
Whipple’s disease
Congenita! Diseases
Acute rheumatic fever pneumonitis
Mickety-Wilson disease (pulmonary dysmaturity) Asthmatic changes
Fibrocystic disease of lung (mucoviscidosis)
 \OL. 104, No. Radiology and Hone’s-comb Lung Disease 813

a differential diagnosis. These possible

causes are of a hearsay variety-those
which “someone has said” can result in a
honeycomb pattern, but which are seldom
seen. The definite and possible causes
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illustrated here are pathologically verified

and are presented to aid in the discussion
of differential diagnosis.

DEFINITE CAUSES OF HONEYCOMB LUNG

FIBROSIS

Fibrosis from whatever cause and its

associated emphysematous changes pro-
duce a reticular pattern (Fig. 3 and ) and
are the most common bases for honeycomb-
ing.’ Bronchial wall fibrosis and sacculation
produce a more worm-eaten appearance
(Fig. ). These diseases are chronic end
results of pulmonary changes and show
little modification in appearance over pro-
longed periods unless a superimposed in-
fection occurs. FIG. 4. Bullous emphysema (vanishing lung disease).
The irregular blebs and bullae compress the ves-
sels into a crowded group of irregular honeycombs.

ACUTE INFECTIONS

The acute infections producing a honey-

comb appearance are usually viral rather

FIG. 3. Chronic fibrosis and emphysema. The hy-

perlucent lung and flat diaphragms indicate the
air content of the emphysematous spaces. The FIG. 5. Bronchiectasis. This multicystic, chewed-up
loss of vascular patterns and irregular linear appearance is the end result of severe influenza
reticular markings of fibrosis honeycomb the and pneumonia. The saccular ectatic areas reveal
“empty spaces.” multiple air fluid levels.
 814 T. H. Johnson, Jr. DEcu.ls,.R, 1968
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I in. . (allpin c)nstinij)tnfl. l’his iisscminated

tit lieretiI (itS flCiI 11(0 1 Sh( )\VS C( )flS( (1 Ia Vt ( n in the
11G. 6. Viral pneumonia. The nodular honeycomb ri Lh t 1(111 L. lIlc I e ft 111 1 in flt4 dent ((0 strates the
appearance is a combination of an alveolar and an patchy nnitiiir intitrates rcsiiitlni. in a Percep-
interstitial pattern with the interstitial pattern tible honeycomb pattern.
predominating. The disease here was acute in-
fluenza.

than bacterial (Fig. 6). The bacterial

pneumonias tend to be predominantly
alveolar and consolidative.7 The viral
diseases have both an interstitial and an
alveolar component with the interstitial
predominating. The acute phase of the
infectious granulomas may have a reticular
punched-out appearance (Fig. 7), and all
of the acute infectious causes of honey-
combing demonstrate a rapidly and fre-
quen tly changing pulmonar\ pattern

CHRONIC REACTIVE 1)ISEASES

The chronic reactive diseases, e.g., lipoid

pneumonia (Fig. 8) and pneumoconiosis
(Fig. 9) produce a true fibrotic honey-
combing. The pulmonary pattern may pass
through a miliary phase, but results in a
true fibrosis and emphysema. Chronic
lipoid pneumonia (Fig. 8) produces a reac-
tion primarily in the lower lung fields, and I in. . liptini Inelllllllia. lies eLierI ale ciii
till ci her ((ii 0 li( (5 Ir js tr( In ii leral
verification of the diagnosis is made by
Ilie rusit1tin dir tie Iijt ii pneizninni,i is t trite
identification of lipophages or abundant jtilinnnare reacti((n tn iii irritative itateri;il. I )ii
sudanophilic material in the sputum.’2 The to th ispiratioonai irhi of introoitictioon, the
pulmonary response to the reactive dusts reaction is usually in the lower lobes.
 \or. 104, No. Radiolog and Hone’comb Lung Disease 8i#{231}

(Fig. 9) commonl’ ends in interstitial

fibrosis with honeycombing; however, it is
accompanied by other lesions including (us-
sem i n ated nodules and conglomerate
masses.5 This picture is most frequentl
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identified in silicosis, but is common to

all pneumoconioses.

CHRONIC GR\NULOMA1OUS DISEASES

The chronic granulom atous diseases clas-

sically produce a honeycomb lung. \Ve
most frequently identify infectious grantl-
lomas such as histoplasmosis (Fig. io) or
tuberculosis; however, other fungi, sar-
coidosis (Fig. ii), etc., must not be forgot-
ten (Table i). The chronic infectious granu-
lomas (Fig. io) are most suspect when the
reaction is in the upper lung fields or
superior segment the of lower lobes. Pul-
monary sarcoidosis (Fig. ii) usually pro- FIG. TO. Chronic granulomatous
disease. The wide-
gresses from an interstitial nodular form of spread fibrosis, and emphysema
retraction, seen
the disease to diffuse interstitial fibrosis and here are typical of histoplasmosis. Tuberculosis
usually shows a more calcific reaction.
honeycombing. The interstitial fibrosis is
irreversible and continues slowly to exten-
sive bullous emphysema.’ differentiated from a number of infectious
or very rare lesions.1 Two primary chag-
CONGENITAL DISEASES
noses evolve in this category. Pulmonary
The congenital causes of a honeycombed dysmaturity (Mickety-\Vilson syndrome)2
lung at the time of first observation must be is characterized by a diffuse, bilateral,
coarse, lace-like pattern of infiltrates with

FIG. 9. Silicosis. Note the interstitial nodulation,

marked fibrotic stranding and early conglomerate FIG. II. Sarcoidosis. Honey-combing is seen here
masses on this chest roentgenogram of silicosis. primarily in the mid and lower lung fields with
No egg shell calcifications are present in the hilar bullous formation predominating in the apices.
areas at this time. The hilar enlargement represents lymph nodes.
 8i6 T. H. Johnson, Jr. DECEMBER, 1968
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I iti. \liicnviscihoss jotihiitoonarv cystic fihrosis.

Pill mona rv fl ant festa tt oTis in tills systemic disease
are resultant from the congenital mucous abnor-
mality. Widespread emphysema with linear
fibrosis and focal atelectasis are manifest. There is
usually a poor resistance to secondary infection.

to their vascular effect--either direct or

FIG. 12. Pulmonary dysmaturity (Mickety-Wilson from abnormal blood proteins, hypersensi-
syndrome). Pulmonary dysmaturity is character- tivity, etc.5 A vasculitis pattern emerges
ized by a diffuse, bilateral, coarse, lace-like pattern that is probably identifiable at Some time
of infiltrates with alternating cystic foci from 2 to
10 mm. in diameter.

alternating cystic foci from 2 to 10 mm. in

diameter (Fig. 12). Roentgenographic clear-
ing of the pulmonary abnormalities occurs
in surviving infants over the first 8 to 10
months. Mucoviscidosis (Fig. 13) is a pul-
monary reaction to a mucous or surfactin
abnormality. The earliest roentgen mani-
festations are emphysema followed by focal
atelectasis from bronchial plugging. The
resultant pneumonitis and continued focal
collapse produce the stringy fibrosis and
patchy densities with which we are more
familiar. Congenital lobar cystic disease of
the lung probably should not be a part of a
differential diagnosis of honeycombing,
for its appearance is bizarre and easily
separable.
FIG. 14. Scleroderma. Cardiomegaly may be totally
vascular or may contain a component of pen-
COLLAGEN DISEASES
cardial fluid. The lungs show diffuse emphysema
All collagen diseases have been impli- but the inferior areas demonstrate a diffuse sclero-.
cated as a basis for pulmonary changes due cyStic appearance.
 VOL. 104, No. 4 Radiology and Honeycomb Lung Disease 817
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FIG. 15. Peniartenitis

nodosa. The lungs reveal an in-
It
creased and the vessels
lucency proceed toward
abrupt ends. The nodular pattern is interspersed
with honeycomb cy-stic areas. FIG. 17. Rheumatoid lung disease. This patient with
clinical advanced rheumatoid arthritis also ex-
hibits the advanced pulmonary findings. The
in the course of all of the collagen diseases, nodular densities are probably rheumatoid nod-
if roentgenograms could be obtained at the ules. The cystic honeycombing results from necrot-
proper times. There is an overlapping of ic nodules and fibrosis from vasculitis.

clinical symptom atology and roentgen find-

ings that confuses the exact identification comb fibrotic pattern should suggest this
of the specific causal entity in some cases; group of diseases. Scleroderma (Fig. 14)

but the appearance of small nodular densi- produces a typical “scierocystic” appear-
ties with a shifting pattern, pleural and
pericardial effusions, and, finally, a honey-

11G. i6. Lupus erythematosus. Pleural reaction and FIG. i8. Pulmonary metastases; carcinoma of right
fluid are present on the left, and peripheral den- lung with lymphatic spread. The pattern of
sities probably represent subsurface infarcts. The malignant spread is both nodular (hematogeneous)
lower lung fields demonstrate the honeycomb and linear (lymphatic). The combined result is a
lesion. honeycomb visualization.
 8i8 T. H. Johnson, Jr. l)FcfSIHFk, 1968

extension.’ The hematogeneous spread will

exhibit varying sized nodules due to the
waves of tumor emboli arriving in the lungs
at different times; l’mphangitic spread is
more uniform. Iymphomas are more likely
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to have associated adenopath’ and medias-

tinal masses than disseminated carcinoma.

RARE CAUSES

The term “rare causes” in this instance

refers to entities that either cannot be
easily grouped in other areas of a honey-
comb differential diagnosis or are infre-
quent in occurrence. Tuberous sclerosis
(Fig. 19), m-omatosis, leiomvomatosis,
and adenomatosis are considered similar
in basis b some investigators and dis-
similar by others.7” The pulmonary char-
acter ma be inseparable by appearance
alone. The basis of these lesions is an in-
crease of the mvomatous elements in the
lungs with or without fibrosis.’ The term
l1G. 19. Tuberous sclerosis. The pulmonary honey-
Hamman-Rich s-ndrome (Fig. 20) has
comb appearance with isolated nodules and a
“shaggy-” heart, often without clinical symptoms,
come to be best understood as an intersti-
is characteristic of tuberous sclerosis. The chest tial fibrosis of unknown etiology rather
roentgenogram is usually less involved than in this than completely idiopathic. Felson5 ac-

case. cep ts the term, H am m an- Rich s v n I rome,

it it is understood to indicate the end-result
ance with a fine honeycomb pattern

thought to be characteristic.5 Periarteritis

nodosa (Fig. 15) is predominantly a lo-
calized vasculitis resulting in loss of pul_
monar’ vessels which may be rapidl\ fatal.
Lupus erthematosus (Fig. i6) is recog-
nized by changing patches of pulmonary
edema and hemorrhage followed by a
linear and fibrotic pattern similar to a
honeycomb. Rheumatoid lung disease (Fig.
17) is probably more common than usually
identified because it is infrequently sus-
pected. The most common lesion is pleuritis
with pleural effusion. Subsequently the
h ng demonstrates rheumatoid nodules
with resultant fibrosis and subpleural cystic
areas 16

MALIGNANT DISEASES
I- in - 20. Hamman-Rich sndrome. Idiopathic diffuse
All malignant causes of honeycomb lung
interstitial fhrosis (1 lamman-Ricli sndrome) is
have a similar basis (Fig. i8). The malig- the prototype for a honevcomli lung pattern.
nant lesion appears in the lungs through a Note the thickened septa and uniformity of the
hem atogeneous spread or lymphangiti c cystic areas.
 \OL. 104, No. Radiology and Honeycomb Lung Disease 819

of a number of conditions and not a specific

entity. The roentgenographic appearance
(Fig. 20) is classic for pulmonary honey-
combing and fibrosis.
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STORAGE DISEASES

The storage diseases should be considered

together, as we cannot identify the stored
material from roen tgenographi c visu aliza-
tion. Eosinophilic granuloma (Fig. 2!) is a
classic consideration for the histiocytosis
storage group of diseases.21 The essential
disturbance is expansion in the reticuloen-
dothelial system and in all organs including
bone, liver and splenic lymphatics. Lungs
may be involved either singly or in combi-
nation.2#{176}

POSSIBLE CAUSES OF HONEYCOMB LUNG

FIG. 22. Hemosiderosis. The diffuse granular pattern
The list of possible causes of honeycomb of this case of idiopathic pulmonary’ hemosiderosis
lung (Table ii) is compiled from reference visually’ resolves as a honeycomb pattern. The
material and occasional examples which orderly rounded lucencies are best seen in the
lung fields.

appear to present a honeycomb appear-

ance. Pulmonary hemosiderosis (Fig. 22),

rheumatic heart disease with pulmonary

edema (Fig. 23), and asthmatic changes
(Fig. 24) are such cases. Pulmonary deposi-

FIG. 2!. Eosinophilic granuloma. The pulmonary’

4
FIG. 23. Rheumatic heart disease with acute pul-
involvement in eosinophilic granuloma is usually monary edema. The mitral valvular disease heart
in the mid or upper lungs with honeycombing in configuration is an indication of a vascular basis
these areas. The pleural reaction in the right for the pulmonary’ disease. The shifting edema
diaphragm area seen here is resultant of a pul- gives a honey-comb pattern best seen here in the
monary biopsy. left hilar area.
 820 T. H. Johnson, Jr. DECEMBER, 1968

Clinical information of dust exposure or

occupation may direct diagnostic investi-
gation. Age is the important factor in
diagnosis of pulmonary dysmaturity. Phys-
ical findings of skin changes, lymph node
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enlargement, or body habitus may narrow

the field of investigation. It is always im-
portant to obtain previous laboratory data
and roentgenograms for comparative evalu-
ation.
Roentgenologic indicators are important
considerations. The speed of apparent
change or lack of change of the pulmonar\’
appearance may direct investigation. Cer-
tain pulmonary areas of primary involve-
ment in the apices or bases indicate specific
etiologies. Despite these indications, pul-
monary biopsy is usually necessary for
definitive diagnosis. The radiologist may
direct the site of biopsy for optimal results.
11G. 24. Asthmatic changes. The left lower lung field
shows a localized honeycomb appearance. The re-
SUMMARY
maining lung fields reveal hyperaeration.
A honeycomb lung pattern is encoun-
tion of hemosiderin with associated fibrosis tered in a significant number of diseases.
is rare but represents a cause of honeycomb- The clinical information must be combined
ing that is stable and unchanging over with the roentgen findings for accurate
prolonged periods of time (Fig. 22). Car- diagnosis, and the more common causes
diac failure, from whatever cause, with should be considered first and eliminated
shifting pulmonary edema infiltrates will before proceeding to the rare diagnoses.
give a sieve-like appearance to the lung Roentgen specifics are varied within the
(Fig. 23). The vascular congestion is an honeycomb pattern and may direct the
indication of this basis. Asthma (Fig. 24), investigation. Examples of causative con-
with its expiratory obstructive component, ditions and differential points are discussed.
bronchial plugging, and focal atelectasis,
Department of Radiology
produces shifting densities in the lung that
University of Tennessee
result in a reticular appearance. College of Medicine
86g Jefferson Avenue
DISCUSSION Memphis, Tennessee 38103

The diagnosis of specific causes of honey-

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