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879

The Radiologic Distinction of


Cardiogenic and
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Noncardiogenic Edema

Eric N. C. Miln& Improvement in the ability to determine the specific cause of any given case of
Massimo Pistolesi2 pulmonary edema would lead to more rapid and definftive treatment “Wedge” pressures
Massimo Miniati2 and measurements of cardiac output derived from Swan-Ganz catheterization assist in
making this determination, but the procedure is invasive, expensive, associated with
Carlo Giuntini3
complications, and not infrequently inaccurate. A plain chest film is, however, almost
invariably available in all patients with pulmonary edema, and as shown in this study,
the cause of the edema can be determined with a high degree of accuracy by careful
attention to certain radiographic features. An independent two-observer study was
performed on 216 chest radiographs of 61 patients with cardiac disease, 30 with renal
failure or overhydration, and 28 with capillary permeability edema. Three principal and
seven ancillary features have been identified, all of which are statistically significant
and permit the cause of the edema to be determined correctly in a high percentage of
cases. The three principal features are distribution of pulmonary flow, distribution of
pulmonary edema, and the width of the vascular pedicle. The ancillary features are
pulmonary blood volume, peribronchial cuffing, septal lines, pleural effusions, air bron-
chograms, lung volume, and cardiac size. Differing constellations of these features
occur, each of which is characteristic of a specific type of edema. Overall accuracy of
diagnosis in this study ranged from 86% to 89%. The highest accuracy was obtained in
distinguishing capillary permeability edema from all other varieties (91%), and the lowest
in distinguishing chronic cardiac failure from renal failure (81%).

Development of pulmonary edema (increased extravascular lung water) is a


common and sometimes life-threatening clinical problem, particularly in critical-care-
unit patients. There are three principal varieties: cardiac, commonly resulting from
Received July 24, 1984; accepted after revision
January 18, 1985. myocardial or valvular heart disease; overhydration, usually caused by excess
This work was supported in part by C.N.R. (Ital-
saline effusion or renal failure with retention of salt and water; and capillary
ian National Research Council) National Cardio- permeability, which can be caused by a wide variety of pathologic, traumatic, and
respiratory Group grant CT 80.0051 6.04, by C.N.R. infective conditions resulting in injury to the pulmonary microvasculature.
grant 104360.04.800381 5, and by the Department
of Radiological Sciences, University of California, The three principal mechanisms of edema formation are (1) increased hydrostatic
Irvine. Part of this work was carried out in the pressure gradient across the capillary wall, (2) diminished osmotic pressure gradient
C.N.R. Institute of Clinical Physiology while E. Milne
across the wall, and (3) increased capillary permeability (damage to the endothelial
was a Fogarty Senior International Fellow, and part
in the Department of Radiological Sciences, Univer- cell junctions, which permits both fluid and large molecules to leak out of the
sity of California, Irvine, while M. Pistolesi was vessels). Change in plasma oncotic pressure is usually a contributory rather than
Visiting Associate Professor.
a primary cause of pulmonary edema. A fourth, and often neglected factor, is the
‘Department of Radiological Sciences, University
of California Medical Center, 101 City Dr. S., Or-
ability of the lymphatics to remove excess extravascular lung water (EVLW). Figure
ange, CA 92668. Address reprint requests to E. N. 1 shows that the balance of forces across a pulmonary capillary wall results in
C. Milne. continual transudation of water into the interstitial space [1]. The excess water
2ItaJii National Research COUnCIl (C.N.R.) In-
passes into the peribronchial/vascular sheath and flows centrally toward the
stitute of Clinical Physiology, 56100 Pisa, Italy.
lymphatics, which normally carry it back to the systemic veins (fig. 2) [2]. Increasing
3Second Medical Clinic, University of Pisa, production of EVLW secondary to changes in transmural hydrostatic and/or cofloid
56100 Pisa, Italy.
pressure results in progressive accumulation of fluid within the interstitial space.
AJR 144:879-894, May 1985
0361 -803X/85/1 445-0879
The junctions between alveolar epithelial cells are “tight” and initially prevent this
© American Roentgen Ray Society water from passing into the alveoli. It therefore flows along the path of least
880 MILNE ET AL. AJR:144, May 1985

Pulmonary edema cannot be detected at an early stage or


Alveolus quantitated accurately by physical examination alone [3-51,
and several noninvasive techniques have therefore been de-
veloped, which attempt to detect edema by assessment of
its effects on the physical properties of the lungs [6-111. None
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Lymphahc of these methods has proved to be useful in the clinical


environment.
Invasive techniques, including indicator dilution measure-
ments of EVLW, have achieved little Success, since the
techniques used have either been inaccurate or too complex
for routine use [3, 12, 13]. Extravascular lung thermal volume
measurement [14, 151 does appear to be accurate enough to
Alveolus be of clinical value but is still invasive, and there are some
important unanswered questions about the validity of using
heat as an indicator.

Fig. 1 -Fluid and solutes pass in both directions across capillary endothe-
hum, but there is net outward flow so that there is always extravascular water Determination of the Cause of Edema
present in normal lung. Tissue osmotic and hydrostatic pressures that dictate
this exchange cannot be measured accurately in interstitial space, and figures Currently, neither external detection nor dilution methods
of 7.0 mm Hg pressure out and 3.0 mm Hg “in” are derived from data in
literature, not measured (1, 21. For simplicity, diagram shows water being
can differentiate among cardiac, overhydration (including renal
reabsorbed only at venous end of capillary (Starling’s original concept), but this failure), and capillary permeability edema. New techniques
has not been proven. Exchange in both directions probably takes place along designed to detect increased permeability of lung microves-
entire length of capillary. Note “tighr alveolar epithelial junction (A) and “lOose”
endothelial cell junction (B). sels and measurements of protein content in pulmonary
edema fluid may assist in this differentiation, but these meth-
ods are not easily used in daily routine practice [16-21].
Usage of the Swan-Ganz catheter is increasing rapidly in
critical care units, and indices of left ventricular end-diastolic
pressure, as represented by the “wedge” pressure, and car-
diac output certainly provide a valuable clue as to the type
‘Cuffing”
and management of edema. Swan-Ganz catheterization re-
mains, however, an invasive procedure with some morbidity,
including pneumothoraces, extrapleural hemorrhage, endo-
cardial injury, infarction distal to the catheter, etc. [22]. False
readings may occur due to failure to wedge, clot within the
lumen of the catheter, kinking of the catheter, failure to place
the tip of a catheter in zone 3, changes in lung compliance
due to severe chronic lung disease or adult respiratory dis-
tress syndrome, and the effects of high levels of positive end-
expiratory pressure (PEEP) [23]. For these reasons and also
because of its expense, the use of Swan-Ganz catheters
routinely has some disadvantages.
:luid tronsudation

Fig. 2.-Diagram of peribronchovascular sheath surrounding bronchus,


arteriole, capillary bed, and venule. Large arrows indicate excess water passing
out of capillaries into interstitial space and into penbronchovascular sheath to Radiologic Detection and Differentiation of Edema
produce peribronchial ‘cuffing.’ Initially, tight alveolar epithelial cell junctions (A
in fig. 1) prevent fluid from passing into alveoli, but as pressure within peribron- In contrast to the techniques described above, the nonin-
chovascular sheath rises, “interstitial tamponade’ occurs, pressure rises, and vasive and readily available chest radiograph has been shown
fluid then passes into alveoli.
to be of considerable clinical value in the detection of edema
[24, 25]. The ability of the radiologist to quantitate edema
from the chest radiograph was first demonstrated objectively
resistance, centrally, producing a peribronchial “cuff” of fluid by Milne [26], who compared assessments of extravascular
and, since the interstitial space is a continuum throughout the lung water made from the chest film with simultaneous meas-
lung [2], may also flow peripherally, producing thin sheets of urements using the Chinard indicator dilution technique [12].
fluid between the lobules, manifested on the chest radiograph Later studies by Pistolesi and Giuntini [13], using a systematic
as Kerley lines. In contrast, capillary permeability edema has and more objective approach to the radiograph and an im-
quite a different sequence of appearance, becoming alveolar proved indicator dilution technique, confirmed this work. Fur-
much more rapidly and passing neither centrally nor periph- ther support for the ability to quantitate pulmonary edema
erally. We offer a hypothesis for this different radiologic ap- from the radiograph has been supplied by Van de Water et
pearance in the Discussion. al. [27], Nobel and Siniewicz [28], and Snashall et aI. [29]. At
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 881

present, the chest radiograph is the only practical method of patient’s instrumental evaluation. We analyzed 122 radiographs in
detecting pulmonary edema at an early stage and following the 61 patients of group 1 , 50 in the 30 patients in group 2, and 44
in the 28 patients in group 3. All cardiac and renal patients were
its evolution accurately [30]. The validity of the radiographic
filmed with a posteroanterior(PA) projection at a 6 foot(2.7 m) anode-
method is now widely accepted by clinicians and physiologists
to-film distance (AFD) with the patient either erect or seated. Patients
[4, 29-34], and the chest film remains the most frequently
with overhydration or lung microvascular injury were filmed in the
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used clinical method for the diagnosis of pulmonary edema. critical care unit using an anteroposterior
(AP) projection and a 6 foot
However, although radiographic patterns of pulmonary (2.7 m) AFD. Most supine films were taken in a special x-ray unit
edema in cardiac, renal, and capillary permeability edema attached to the physiology laboratory at the University of Pisa and a
patients have been described [1 4, 26, 35-58], there has not 6 foot (2.7 m) AFD was used. The remaining supine films, obtained
been a definitive study of the value of the chest radiograph in at the University of California, Irvine, were made at 40 inches (1 m)
determining which type of edema is present in any given case. AFD. All 30 of the overhydration cases were filmed erect. Thirty-six
Clearly in many instances the history, signs and symptoms, of the injury lung films were supine and eight erect.
The effects of position and projection on vascular pedicle width
and clinical course of the patient’s disease will be sufficient
and cardiac size have been reported elsewhere [59-61]. We believed
to establish the cause of pulmonary edema, but there remains
initially that position and projection would have an effect on our ability
a large proportion of cases, particularly in critical care units,
to distinguish between cardiac and noncardiac edema; therefore, we
where the cause of the edema may be very difficult to
analyzed the statistical significance of vascular pedicle width and
determine. For example, patients with sepsis who are being cardiac size, both corrected for position and projection and uncor-
vigorously treated by systemic antibiotic therapy may develop rected. The results of the corrections for cardiac size are reported
pulmonary edema equally well from overhydration, capillary later. We also compared the distribution of blood flow and edema in
permeability, cardiac arrhythmias, or renal decompensation. the injury lung films that had been made supine (36) with those filmed
It is obviously of vital importance for the patient’s physician erect (eight). As anticipated, we found a balanced” distribution of
to know which of these mechanisms or combination of mech- flow in the supine patients. In most erect patients the distribution was
anisms is operating before he can treat the patient definitively. normal. This change in distribution with position is reflected in the
data reported later. In these injury lung cases, there was no difference
On the basis of past clinical experience and experimental
in the distribution of edema in the erect or supine position.”
studies [26, 27, 47, 48, 51 59-61 ], we hypothesized , that
Comparing our ability to distinguish the three groups of edema on
each of the main categories of pulmonary edema (cardiac,
the basis of a!! of the 12 radiologic features assessed, we found no
overhydration, and capillary permeability) had certain radi- statistical difference between the corrected and uncorrected data.
ographic features that would enable us to distinguish it from Since we had demonstrated that it was not essential for the correct
the other varieties. One such feature is the distribution of radiologic distinction of the three types of edema to make these
blood flow on the chest radiograph. For example, in chronic corrections, data reported here are the uncorrected data, and the
the
cardiac failure, the distribution of flow is usually “inverted” level of accuracy of classification into the three categories of edema
(base-to-apex redistribution), in overhydration and renal failure is that achieved without any correction for either the AP and/or supine
it is “balanced” (homogeneous), and in capillary permeability positions.
The 61 patients in group 1 had pulmonary edema complicating
edema it is usually normal [62-65]. In addition to the distri-
either acute myocardial infarction (three patients), ciecompensated
bution of pulmonary blood flow, we chose, on the basis of
chronic left heart failure on the basis of ischemic myocardiopathy
their known relations to certain facets of cardiac function, 11 (21), or mitral valve disease (37). Of the 30 patients in group 2, 20
other factors that we believed would prove to be useful had chronic renal insufficiency and were under treatment by dialysis,
indicators of the type of edema present. The aim of our study and the other 10 had been overhydrated. The 28 patients in group 3
then is to determine, as objectively and rigorously as possible, all had physiologic evidence ofthe adult respiratory distress syndrome
the validity of the chest radiograph in deciding what type of resulting from traumatic (seven patients) or nontraumatic (six) cerebral
pulmonary edema is present, in order to provide a rational lesions, bums of various degrees of severity (five), sepsis (four), or
pathophysiologic basis for the treatment of that particular posttraumatic fat embolism (four), viral pneumonia (one), and amniotic
fluid embolism (one).
type of edema.
Experience indicates that it is easier to decide what type of edema
is present if one can compare sequential films in the same patient,
but since we wanted to find out just how important this temporal
Materials and Methods factor was, in comparison to the analysis of an individual radiograph,
all films had the identification data and film date removed. The films
The study was performed on 216 chest radiographs obtained from
were then coded and mixed randomly before being independently
61 patients with cardiac disease (group 1), 30 with renal disease or
submitted to each of two observers (M. M., E. N. C. M.). After the
iatrogenic overhydration (group 2), and 28 with lung microvascular
injury (capillary permeability edema) of many different causes (group
analysis had been made without temporal (sequential) information,
the films were then placed again in their correct sequence for each
3), who had been admitted to the intensive care units of the Univer-
patient. Each reader was then asked to determine whether seeing
sities of Pisa (Italy) and California (Irvine). To be included in this study,
the films in sequence affected his conclusions concerning the type of
patients were required to have radiographic evidence of pulmonary
edema present.
edema, full clinical and and/or physiologic documentation of the cause
of their edema, and sequential radiologic studies throughout the
. Since capillary permeability edema is proteinaceous and viscid, we hypoth-
course of their hospital stay. Histologic examination of the lungs was
esize that it cannot migrate freely through the interstitial space and believe that
not available except in some lung injury cases.
the lack of change in distribution of edema between the erect and supine
The radiographs used in this study were all of acceptable diagnos- positions is a further diagnostic point toward the diagnosis of capillary perme-
tic quality and were taken as closely as possible in time to the ability edema.

Thj One____
882 MILNE ET AL. AJR:144, May 1985

Ez’tCt Fig. 3.-Actual reading list used by all film


Si). siins or AP O.r* *0 *0 readers. Its use is detailed in text.
. PATIENT PO5lTlOt4:SE:Ssat RUITECHt4IQUE 1.
Jo(
LI. 0**
SR = sponteus PWi?IftW!

2 MODE or VEtfnLAT1OIi AV asstst.4


#{149} ventilatte.
_.
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3 ARTSIZE8’Si4APE: 3
- .N.,

a)Zmpressio* :
b) t1*a.swe,nflt (total)
VASCVLAR PEDcLE C) i$weiaent (t 1.44
4 d Azyos measurJsa or HS a -, T*s)
ei Y*raI msuent
({m. s in ar’ rb.rdero ftt* 2nd rb b tie cnc#{233},)

5 WN& VOLUME {eawi the wsf.ntsrborcl.’of the 2r.4 nb ta the p 4 *ie 5

Not ctwly sw c ‘5)-

6 HILARABNORMAUTIES: Insielsrz. .#{247} k,.,. 6


Inua.n.A 4assity: - - + +4 +44

Blurrinp .-++ 4+4

A bS
a PULt1OP4AP./ - . ++ 4+9. a
#{149}
9 PIbRO$MLI4L GUFFIN 0 + + 4+ 4+4 [Ma .d 3

SEPTM. LJi4E.S { 0 O-++ +4’ 41+


j’
11 wiDer-iIN oF FI$SURSS 0-J) + 1+ +4+

- fr#{188}perievul
WPIe )EHSiT INcQEi15-, DtcFUS centml -- - + 4+ +4

t=e1en . (,t.

13
L.u.14 XEMsrry ,r4CREt1NT PATCH)’ (I)I:’: Slrebk 13

AIR 5R0MC404RJu% : O-’I+ 44.1+4 {rt .

COtIMEI4T5

To introduce as much objectivity as possible into our analyses we Line 3. -Heart shape was characterized as shown in figure 3. The
constructed an interpretation guide (fig. 3), which each of the readers right heart border was divided into two segments, (1) superior vena
had to use in the analysis of every film. The reader had to respond cava and (2) right atrium, and the left border into four parts, (3) aorta,
to 14 set tasks, either to measure a specified organ at a specified (4) main pulmonary artery (MPA), (5) left atnal appendage, and (6) left
dimension (e.g., the width of the azygos vein) or to say whether a ventricle. At each point, the observer was asked to estimate size
certain feature was or was not present (e.g. , penbronchial cuffing) or from (reduced) to +++ (grossly
- enlarged). The cardiothoracic ratio
to grade the changes (graded from 0 to +++) and to indicate where was measured as shown (fig. 3).
the changes had occurred (U upper, M = middle, L = lower lung
= Line 4.-We have shown elsewhere [26, 59, 60] that the width of
zones). Use of the guide is described below; each number corre- the vascular pedicle is closely related to the systemic blood volume,
spends to a line on the interpretation guide (fig. 3). and that change in width of the pedicle is closely related (r 0.96, p =

Line 1.-The patient’s position was recorded (e.g., erect, seated, < 0.001) to change in systemic blood volume [60J. The readers were
lordotic) whether the film was PA or AP. If rotation was present, the asked to give an impression first of the size of the pedicle as normal
degree and direction was indicated by a small sketch showing a (+), diminished (-), or enlarged (++, +++) and then to measure it
spinous process and the ends of the clavicles. and the azygos vein.
Line 2.-The mode of ventilation was recorded, and if assisted Line 5.-Lung volume was represented arbitrarily by a single linear
ventilation was being used, the peak inflation pressure and level of measurement from the lower border of the right second rib to the
PEEP were recorded. highest point of curvature of the diaphragm.
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 883

Line 6.-Hilar abnormality: The reader was asked to say whether TABLE 1: Interobserver Variability: 216 Chest Films, Two
the hilum was normal or not, and if not, to characterize the abnormality Observers
in terms of size, density, and clarity of the margins of the hilar
Disagreement
structures. in (%)
Line 7.-Blood flow distribution was represented by three Heart size 11
sketches labeled A (normal), B (balanced or homogeneous flow), and Vascular pedicle 2 ±
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20

C (inverted). The reader compared the distribution on the film with Pulmonary blood flow distribution 29
the sketches and entered A, B, or C. If the distribution did not fit A, Pulmonary blood volume 26
B, or C, the reader was asked to sketch in the actual distribution of Septal lines 8
flow in the blank chest outline provided (D). Peribronchial cuffs 8
Line 8.-The reader was asked to assess the quantity of blood in Air bronchogram 19
the lungs from - (reduced) to +++ (markedly increased) [51 , 62]. Lung density increase 6
Lung edema, regional distribution 8
Line 9. -If no peribronchial cuffing was present, the reader entered
0. If cuffing was present, he was asked to quantify it from + to +++ Mean average variation e measurement.
and to indicate where it occurred in the lung (+ = bronchial wall
minimally thickened but definitely detectable, ++ = moderate thick-
ening, +++ = gross thickening).
Line 10.-If septal lines were present, they were quantified from The prevalence of each of the 12 radiologic findings observed in
+ to +++ and their position noted. each of the three types of edema was compared by a chi-square test
Line 1 1 . -The reader noted whether the fissures visualized were (exact test of Fisher). We accepted p <0.05 as indicating statistical
normal or widened and quantified t’te de “ee of widening from + to significance.
+++.

Lines 1 2 and 13. -The reader was asked to record whether the
edema was distributed homogeneously or patchily, whether it was in
the upper. middle, or lower lung zones, and to state specifically Results
whether it was peripheral, central, or evenly distributed from the chest
Interobserver Variability
wall to the heart. If the distribution of edema could not be described
in these terms, a blank chest outline was provided for the observer Table 1 shows the percentage disagreement between two
to add a small sketch of the distribution of edema. observers in various required information extraction tasks.
Line 14.-Air bronchograms were classified as present or absent,
Findings that simply necessitated measurement, such as the
their extent assessed (+ to +++), and their position (upper, middle,
cardiothoracic ratio or vascular pedicle width, had a very low
or lower lung zones) noted (4- = one small area only involved, ++ =
mean average variation (2%), but some visual assessments,
one large or several smaller areas in one lung involved, +++ = both
lungs involved). such as those of pulmonary blood flow distribution and pul-
Finally, the reader was asked to state specifically what type of monary blood volume, had a much larger percentage of
edema was present. Initially the criteria used to make this decision disagreement (29% and 26%, respectively). However, the
were those with which we had had experience (principally blood flow interobserver disagreement in the final diagnosis was only
distribution, vascular pedicle width, and cardiac size), but as the work 8%. The explanation for this is shown in table 2. Each of the
proceeded, the value of other criteria, such as the presence of air statistically significant features used in analyzing the radi-
bronchograms and the presence or absence of penbronchial cuffing ograph was looked at in each individual film (from 1 to 216).
and septal lines, became evident and these were included in our
Concurrence between the two observers for each of the
judgments. Therefore, a learning process took place as the work
factors was designated + and disagreement In film 1 (table
-.
proceeded, and it could reasonably be anticipated that a prospective
2), there was disagreement about the pulmonary blood vol-
study, based on the expanded criteria finally chosen on the basis of
statistical analysis, would show an even greater level of accuracy ume but agreement in nine other factors; therefore, the same
than that reported in this study. Space was provided to make written diagnosis was made by both readers. In case 5 (table 2),
comments; for example, if the reader thought some discrepant find- there were two disagreements, about pulmonary blood flow
ings were present or that more than one type of edema was present, distribution and about the presence of air bronchograms, but
he was asked to list the reasons for saying this. there was agreement about the other eight features and
therefore no disagreement about the diagnosis. Clearly, when
there are so many features that have statistical significance
Data Analysis in distinguishing one type of edema from another, a fairly high
Interobserver agreement or disagreement in recognizing the var- degree of interobserver variability in any one feature can be
ious radiographic findings was assessed for the 21 6 chest radi- tolerated without influencing the final diagnosis.
ographs read independently by two observers. Interobserver agree- Both observers agreed and made the correct diagnosis in
ment was considered to be present when both recognized a radi- 82% of the cases, and both observers agreed but were
ographic sign (e.g., peribronchial cuffing) or the same qualitative incorrect in 1 0% of the cases. After placing the films in their
characteristic of a radiographic pattern (e.g., redistribution of pulmo-
correct temporal sequence and reconsidering their diagnoses
nary blood flow). The grading of the various radiographic findings
(but still without knowing the clinical diagnosis), an incorrect
was not considered in the judgment of agreement. Interobserver
diagnosis was changed to a correct one in 3% of cases,
disagreement posed the problem of which reading to use in analyzing
the relative prevalence of each radiologic finding in the three types of increasing the final figure for a correct diagnosis with agree-
edema. We approached this by reexamining the chest films in ques- ment by both observers to 85%. The more experienced reader
tion and obtaining a consensus from all of the authors analyzing the made the correct diagnosis in 89% of cases and the less
radiograph simultaneously. experienced in 86%. The highest accuracy was achieved in
884 MILNE ET AL. AJR:144, May 1985

TABLE 2: Interobserver Variability in Individual Cases: 216 Chest Films, Two Observers

Film No.

1 2 3 4 5 6 7 ... 216

Heartsize + + + - + + + ... +
Vascular pedicle + + + + + + + ... +
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Hilar abnormalities + + + + + + + ... +


Pulmonary blood flow distribution .. + + + + - + + ... +
Pulmonary blood volume - + + + + + - ... +
Septal lines + + - + + + + ... +
Peribronchial cuffs + + + + + + + ... +
Air bronchogram + - + + - + + ... +
Lung density increase + + + + + + + ... +
Lung edema, regional distribution .. + + + + + + + ... -

Note-Agreement (+). disagreement (-).

Fig. 4.-Distribution of pulmonary blood flow:


A, Normal; occurs principally in capillary permea-
bility edema. B, Balanced; occurs principally in
overhydration or renal failure. c. Inverted; occurs
principally in cardiac failure.

A B
C

PULMONARY BLOOD FLOW DISTRIBUTION Fig. 5.-Histogram showing relative percent-


ages of normal, balanced, or inverted flow distri-
bution in cardiac, renal, or injury (capillary perme-
ability) edema. Dots indicate statistical signifi-
Normal Balanced Inverted cance between columns.

cardiac
renal

.
IJ injury
0
.
1 #{149}-Q.Q5
#{149}.-OO1 Significance
0
...-o.oo1J
.

distinguishing capillary permeability edema from cardiac or normalities) were found to have little or no statistical signifi-
renal/overhydration edema (91 %) and the lowest accuracy in cance in distinguishing the three types of edema and will not
distinguishing chronic cardiac failure from renal failure (81 %). be discussed further.
Of the 13 factors that were initially analyzed, four (lung The three principal radiologic factors that had the greatest
volume, heart shape, widening of the fissures, and hilar ab- statistical significance in determining which type of edema
AJR:144. May 1985 RADIOLOGIC DISTINCTION OF EDEMA 885

Fig. 6.-Distribution of pulmonary edema.


There are three principal patterns, each of which
corresponds to specific type of edema: A. Even:
principally basal (gravitational) and homogeneous
from chest wall to heart but with perihilar com-
ponent also. Principally occurs in cardiac edema.
B, Central; occurs principally in overhydration or
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renal failure. C, Peripheral; markedly patchy-it


often spares costophrenic angles. Note air bron-
chograms. This type of distribution occurs almost
exclusively in capillary permeability.

A B C

Fig. 7.-Histogram showing relative percent- REGIONAL DISTRIBUTION OF LUNG EDEMA


ages of three different distributions of edema in
cardiac, overhydration (renal), and injury (capillary
permeability) lung edema.
CENTRAL PERIPHERAL EVEN

- cardiac

#{149} renal
#{149} #{149} #{149}
#{149} #{149}
#{149} ci injury
r r
Significance

0 #{149}-O05
#{149} #{149}
.-o.o 1
#{149}#{149}
#{149}-o.oo1

was present were the distribution of pulmonary blood flow, Distribution of Pulmonary Edema
distribution of pulmonary edema, and the width of the vascular
pedicle. Although there were many variations in the distribution of
edema, all of these could be grouped into three principal
categories: even, central, and peripheral (fig. 6). The histo-
Distribution of Pulmonary Blood Flow gram (fig. 7) shows a previously unsuspected sharp demar-
cation of the three types of edema based on the pattern of
There are three principal patterns, each of which corre-
distribution. In cardiac failure the even (homogeneous from
sponds to a specific type of edema (fig. 4). The relative
chest wall to heart) pattern was by far the commonest (90%
prevalence of the three patterns of distribution in each of the
of cases) and only 1 0% were predominantly central (perihilar).
three types of edema, designated cardiac, renal (overhydra-
This finding is somewhat at variance with the commonly held
tion), and injury (capillary permeability), is shown in figure 5.
view that central edema is characteristic of cardiac failure and
In cardiac edema, 50% of patients showed an inverted flow
will be more fully discussed later. The distribution of edema
and 40% a balanced distribution of flow. In renal failure
in the cardiac cases was clearly affected by gravity and was
(overhydration), no patients showed an inverted distribution,
80% had a balanced distribution, and 20% were normal. In
usually densest at the lowest visualized part of the lungs, the
capillary permeability, 40% had a normal distribution of flow costophrenic angles. In the renal/overhydration cases, central
and 50% a balanced distribution. It should be noted that all edema predominated (70% of cases) and no case of periph-
of the capillary permeability patients in the “balanced” group eral edema was seen. In many cases, the costophrenic angles
were filmed in the supine position, whereas all of the cardiac were spared. In contrast with the edema of renal or cardiac
and renal patients were upright. Whenever a capillary perme- failure, the lung injury cases showed a very patchy type of
ability patient was filmed in the upright position, he showed a edema, often with small intervening unaffected patches of
normal distribution of flow. lung, usually sparing the costophrenic angles. Edema was
886 MILNE ET AL. AJR:144, May 1985

Fig. 8.-Vascular pedicle width. There are


three possible variations: A, Normal; commonest
in capillary permeability or acute cardiac failure.
B, Widened; commonest in overhydration/renal
failure and chronic cardiac failure. C, Narrowed;
commonest in capillary permeability edema.
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A B C

VASCULAR PEDICLE WIDTH IN LUNG EDEMA Fig. 9.-Histogram showing relative percent-
ages of three differing vascular pedicle widths in
cardiac, overhydration/renal, and capillary perme-
ability (injury) edema.
<43mm. 43-53mm. >53 mm.

0/0

- cardiac
:: renal
c injury
jgjfjcance:

#{149}-5O per cent


‘I N

is is

Normal VPW (n 83) 48±5 mm.

peripheral in 45% of cases and extended from the chest wall des; only 1 5% were normal. In capillary permeability edema,
to the heart in 35%. 35% of the patients had a normal pedicle and 35% a narrowed
pedicle, even though 60% of the patients were filmed in the
supine position, which increases the vascular pedicle width
Vascular Pedicle Width (VPW)
an average of 20% [62].
There are three possible variations of VPW: diminished, In addition to these three principal factors, we found seven
normal, or increased (fig. 8). Normal (for an erect 70-kg ancillary features that are also of value in determining the type
patient) is defined as 43-53 mm (48 mm ± 1 SD), diminished of edema:
is less than 43 mm, and increased is more than 53 mm [62].
The relative frequency of these three variants is indicated in
Pulmonary Blood Volume
figure 9. In cardiac failure, 60% of the cases showed a VPW
greater than 53 mm and 40% were in the normal range. Most There are three possible variations in pulmonary blood
of the latter cases were either acute failure or cases of mitral volume (PBV): diminished, normal, or increased (fig. 10). A
valve disease, in both of which there is no increase in circu- decrease in PBV is quite uncommon, but was seen in a small
lating blood volume [66, 67]. The renal/overhydration patients percentage of capillary permeability cases on PEEP and in a
showed a high percentage (85%) of widened vascular pedi- few cardiac cases with very low cardiac outputs (fig. 11). In
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 887

Fig. 10.-Pulmonary blood volume. There are


three possibilities: A, Decreased; uncommon in
any of the three types of edema unless positive
end-expiratory pressure (PEEP) is being used. B,
Normal; very common in permeability and cardiac
edema (in cardiac edema, although upper lobe
vessels are larger. lower lobe vessels are smaller
blood volume is therefore normal).
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and pulmonary
Uncommon in overhydration/renal edema. C, In-
creased; very common in overhydration/renal
edema, less common in cardiac edema.

A B C

Fig. 11.-Histogram showing relative percent-


ages of each of the three variations in pulmonary
Pulmonary Blood volume
blood volume in cardiac, overhydration/renal, and
capillary permeability (injury) edema.

100_ Reduced Normal Increased

% - cardiac
#{149} renal
injury
50_ I Significance
#{149}-J5
#{149}#{149}-o.o1
II #{149}-O 001

n Ir-i

general, the PBV tended to be increased in renal failure/ value in differentiating capillary permeability edema from the
overhydration (70#{176}h).
In cardiac cases, the PBV was increased other two varieties. For example, we have never to date found
in only 40%. In capillary permeability edema, an increased septal lines in a case of pure capillary permeability edema.
PBV was unusual (2O%) and most cases (80%) had a normal Similarly, peribronchial cuffing and pleural effusions are much
PBV.t rarer in capillary permeability edema than in the other two
varieties. In contrast, air bronchograms are very common in
capillary permeability (70%) and much rarer (20%) in cardiac
Septal Lines, Peribronchial Cuffing, Air Bronchograms, and
and renal/overhydration edema.
Pleural Ef fusions

Figure 12 shows the value of four other features (septal Lung Volumes
lines, peribronchial cuffing, air bronchograms, and pleural
Lung volumes were usually normal or increased in patients
effusions) in distinguishing what type of edema is present.
with overhydration or renal failure, reflecting the fact that the
None of these factors is of much value in differentiating cardiac
lung is in effect an erectile organ and enlarges progressively
from renal/overhydration edema, but they are of considerable
as the pulmonary blood volume increases. In cardiac failure,
in the absence of obstructive lung disease, lung volumes were
reduced, reflecting the diminished compliance of a wet lung.
t Pulmonary blood volume (PBV) was measured in 28 cardiac patients and
correlated with the radiologic grading.” The correlation coefficient was 0.5 (p In capillary permeability edema, the lung volumes were usually
<0.025). Although there was some overlap in the radiologic differentiation of normal unless the patient was on positive pressure ventilation
normal (450-650 ml) from mild to moderate increase in PBV (650-850 ml),
complete distinction was achieved between normal and markedly increased
with high levels of peak inflation pressure, in which case lung
(>850 ml). volumes became large.
888 MILNE ET AL. AJR:144, May 1985

Fig. 12.-Histogram showing relative percent-


Septa I Pe ri bronchial Air Pleural
ages of visualization of septal lines, peribronchial
lines cuffing bronchograms e ffusions cuffing, air bronchograms, and pleural effusion in
three types of edema.
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cardiac
.:.:renal
injury
50. Significance
-005

#{149}
#{149}-0.01
#{149}
S
#{149}
#{149}
#{149}-0.001

TABLE 3: Radiographic Features of Pulmonary Edema

carciiac Renal Injury

Heart size . Enlarged Enlarged Not enlarged


Vascular pedicle Normal or Enlarged Normal or
enlarged reduced
Pulmonary blood flow distribution Inverted Balanced Normal or
balanced
Pulmonary blood volume Normal or Increased Normal
increased
Septal lines Not common Not common Absent
Peribronchial cuffs Very common Very common Not common
Air bronchogram Not common Not common Very common
Lung edema, regional distribution (horizontal
axis) Even Central Peripheral
Pleural effusions Very common Very common Not common
Note-Each factor listed has been shown to have statist cal significance in determ ineng which type of edem a Is present.

Heart Volume Discussion

One final feature of some value is the heart size as meas- There are several circumstances in which it becomes rn-
ured by the cardiothoracic ratio (CTR). For the 40-inch (1 -m) possible to visualize one or more of the features used to
AP supine films, we applied a correction factor to the CTR to determine the type of edema. In patients with severe lower-
compensate for geometric magnification (CTR corrected = lobe edema, it may be impossible to assess pulmonary blood
[CTR measured - (CTR measured/i 00)] x 1 2.5). This cor- flow distribution. This difficulty is compounded in patients with
rection factor of 1 2.5% was derived from prior experimental ascites and a high diaphragm. Under such circumstances,
studies with both anthropomorphic phantoms and patients in one may not be able to differentiate cardiac from renal/
the PA position at 72 inches (1 .8 m) and in the AP position at overhydration edema. While this differentiation may be quite
72 and 40 inches (1 .8 and 1 m) [61 ]. After application of this readily made on the basis of renal function studies, these may
1 2.5% correction factor, cardiac enlargement (CTR > 0.5) also be compromised in heart failure. However, it is still easy
was found in 85% of renal/overhydration cases and in 72.5% to distinguish such cases radiologically from capillary perme-
of cardiac cases, but in only 32% of capillary permeability ability edema. Capillary permeability edema may also be so
cases. dense and extensive that it becomes impossible to judge
A summation of all the statistically significant factors in pulmonary blood volume or flow distribution, but the presence
distinguishing the three types of edema is given in table 3. of many of the other features of injury lung edema persist,
However, it is much easier to see how different constellations allowing the correct diagnosis to be made. In fact, the occur-
of all the factors described permit the distinction of the three rence of florid edema without peribronchial cuffing and in the
types of edema, than it is to read about them. Figure 13 presence of a normal or narrow pedicle would immediately
demonstrates the classic appearances of chronic left heart make one suspect capillary permeability as the cause.
failure, figure 14 demonstrates overhydration/renal failure, Another common problem is the simultaneous occurrence
and figure 15 demonstrates capillary permeability edema. of two or more types of edema. In such cases, the sequence
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 889
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..i j
A B
Fig. 13.-A, Diagram illustrating usual appearances of chronic cardiac and effusions are all present, indicating free-flowing (nonproteinaceous) edema
failure. Distribution of blood flow is inverted, indicating elevated pulmonary fluid. Air bronchograms are absent. Lung volume is reduced; dashed line
venous pressure. Distribution of edema is basal and homogeneous from chest indicates diminished lung volume secondary to diminished compiiance. Cardiac
wall to heart. Vascular pedicle width and azygos width are enlarged. indicating size is increased. B, 30-year-old patient in chronic left heart failure. Widened
increased systemic blood volume. Pulmonary blood volume is not increased; it vascular pedicle (arrows); enlarged azygos (arrowhead). Peribronchial cuffing
is engorged cranially but diminished caudally. Peribronchial cuffing, septal lines, and redistribution of flow are present.

of events or the occurrence of conflicting features may allow hydrostatically based edema and capillary permeability edema
the suspicion that more than one type of edema is present. can be explained on the basis of the different mechanisms of
For example, a patient may present with the typical appear- edema formation at the microscopic level within the lung.
ances of capillary permeability edema, then, over the next In hydrostatic edema, the first visible site of accumulation
few days, develop a “balanced” distribution of flow, a widened of fluid is in the loose connective tissue around the blood
pedicle, and peribronchial cuffing. These findings would sug- vessels and airways [71 ]. This loose connective tissue space
gest he has superimposed overhydration. Many such different is continuous around the vessels and bronchi, the interlobular
constellations of conflicting features can occur, but if one is septa and the subpleural space [72]. Fluid in the spaces is
familiar with the classic appearances of each individual type shown on the chest radiograph as peribronchial cuffing, Kerley
of edema, it may be possible to diagnose which combination lines, and subpleural fluid accumulation. In hydrostatic and
of edema types is present.t overhydration pulmonary edema, this extravascular fluid can
Despite these difficulties, it is possible, using the criteria be considered a plasma ultrafiltrate, which progressively di-
listed, to determine the cause of pulmonary edema in a high lutes the fluid in the interstitial space around the vessels
percentage of cases. Capillary permeability edema is partic- where fluid transudation is taking place, creating an osmotic
ularly distinctive by virtue of the patchy, frequently peripheral, pressure gradient from the periphery of the lung, where the
nongravitational distribution of edema; the normal heart size, pressure is low, to the center of the lung, where the osmotic
pulmonary blood volume, and vascular pedicle; the normal pressure is higher. Water molecules will move along this
distribution of flow; absence of septal lines; and rarity of osmotic gradient toward the center of the lung, facilitated also
peribronchial cuffing and pleural effusions. Our findings con- by a hydrostatic gradient of pressure between the perimicro-
cerning the peripheral distribution of edema and the absence vascular interstitium and the hilar regions [72-75]. This hy-
of peribronchial cuffing and effusions are consistent with drostatic gradient is at least partially due to respiratory motion
previous observations in injury lung edema [3, 44-48, 56-58, of the lung [69, 72], and a patient with good lung compliance
69, 701. We believe that the marked differences between should (theoretically) be able to pump fluid out of the periphery
of the lungs better than a patient with lungs of low compliance.
This may be a partialexplanation for the central location of
A further useful radiographic feature, which will be the subject of another
paper, is the thickness of the soft tissues along the chest wall. We have shown edema in patients with renal failure,who tend to have more
1681 that change in extravascular body water correlates with changes in soft- compliant lungs than patients with chronic cardiac failure.
tissue thickness. Our observations indicate that increasing or decreasing extra-
vascular body water can be quantified by measuring changes in chest wall Patients with renal failure tend to be younger and have had
thickness. This will assist further in deciding what type of edema is present. less opportunity for respiratory disease than the cardiac pa-
890 MILNE ET AL. AJR:144, May 1985
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Fig. 14.-A, Diagram of usual appearances in renal failure or overhydration slightly increased (dashed line). Cardiac size is usually large: In overhydration
edema. Distribution of blood flow is balanced, indicating large cardiac output this reflects volume overload and disappears on diuresis. In renal failure, uremic
and recruitment of all vessels. Distribution of edema is central. Vascular pedicle myocardiopathy and/or pericardial effusion may also be present and not resolve
width and azygos size are enlarged, sometimes massively, reflecting large after dialysis. B, 36-year-old patient with renal edema. Note central distribution
systemic blood volume. Pulmonary blood volume is enlarged. Peribronchial of edema, balanced distribution of flow, and large azygos vein. Despite pres-
cuffing and effusions are present. Septal lines are present, indicating free- ence of edema, lung volume is normal.
flowing edema fluid. Air bronchograms are absent. Lung volumes are often

tients, who are older. In many of the cardiac patients, at least of the lymphatic system. Recent evidence shows that the
one causative factor in their disease seems to be smoking, clearance of protein-rich fluid is slower than that of nonpro-
and the same group has a high incidence of emphysema and/ teinaceous fluid [79]. We believe that the inability of this
or chronic bronchitis. Clearly, as fluid accumulates within the proteinaceous edema to migrate centrally explains the ab-
perivascular space, a point must be reached at which the sence of peribronchial cuffs, and its failure to migrate periph-
sheath is maximally distended and the pressure increases erally explains the absence of septal lines and pleural effu-
abruptly-a process we suggest might be called “interstitial sions. It also explains why, once the pattern of capillary
tamponade.” At this point, alveolar edema occurs. permeability edema has developed, it tends to stay quite fixed
In contrast to these mechanisms of hydrostatic edema, in on the chest radiograph for days or weeks at a time, unlike
capillary permeability edema, protein leaks through the dam- the variations that occur in hydrostatic edema. In our experi-
aged open endothelial cell junctions (fig. 1), and there is ence, persistence of the peripheral distribution of capillary
therefore a protein-rich fluid accumulation in the interstitial permeability edema is a poor prognostic sign, whereas central
space close to the leaking capillaries, which predominate in migration of the edema pattern seems to be an index of
the periphery of the lung. This same peripheral origin of injury healing.
lung edema is also seen in CT studies of experimental animals Electron microscopic studies of the microanatomy of the
given oleic acid [76], but it is evident on plain chest films pulmonary capillaries show that they are fused on one side
because of superimposition of the “peripheral” densities on only, to the basement membrane of the alveolar epithelial
the AP and PA film (fig. 16). cells [80] (fig. 1). It seems reasonable to hypothesize that
Because of the protein leak in the lung periphery, there is damage to the capillary can simultaneously cause damage to
no osmotic gradient tending to cause fluid to pass from the the alveolar epithelium on the fused side, which may be
periphery to the center; furthermore, the diffusion of water responsible for the rapid development of an alveolar compo-
molecules is rendered difficult by the high oncotic activity of nent in capillary permeability edema, compared with the usu-
the extravasated proteins. The proteins cannot diffuse easily ally delayed appearance of alveolar edema in hydrostatic
through the dense meshwork of fibrils interspersed within the edema.
connective tissue ground substance [77, 78]. Therefore, their Although we have confined ourselves here to the com-
regional clearance is almost completely related to the function monest types of edema, it should be remembered that there
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 891
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A
Fig. 15.-A, Diagram of usual changes in capillary permeability (injury) very common. Lung volume is normal or small, reflecting diminished compliance
edema. Distribution of blood flow is normal; there is no increase in intracardiac (may be large if PEEP is used). Cardiac size is normal or small, reflecting low
pressure to cause inversion and no increase in pulmonary blood volume to cardiac output, particularly if PEEP is used. B, 30-year-old patient with septi-
cause balanced distribution. Distribution ofedema is peripheral and very patchy. cemia and capillary permeability edema. Despite supine position, vascular
Vascular pedicle width and azygos size are normal or small, reflecting normal pedicle is of normal width. Extensive edema, denser peripherally with air
or small circulating blood volume. Pulmonary blood volume is normal (reduced bronchograms but no cuffing, septal lines, or effusions. For supine film, blood
if PEEP is used). Peribronchial cuffing and septal lines are very rare, suggesting flow distribution is normal and there is no increase in pulmonary blood volume.
that increased viscosity of capillary permeability edema fluid makes it impossible Wedge pressure was 8.0 mm Hg.
to flow away from its site of origin. Effusions are rare. Air bronchograms are

are other varieties of hydrostatic, noncardiac edema, including occurs in these cases [48]. Very similar appearances, but
high altitude, neurogenic, and reexpansion edema. The last usually without the dilatation of the pulmonary artery, accom-
15 rarely a diagnostic problem, but the first two often are. pany high-altitude pulmonary edema now reported on many
Once the characteristic appearances of the three basic edema occasions at heights at low as 8000 feet (2500 m) [81].
types are familiar, it becomes possible to suggest or even There is also an atypical variety of capillary permeability
specifically identify other varieties from discrepancies in the edema. Many of the usual features will be found, including
classic presentation. normal pedicle, heart, pulmonary blood volume, and blood
For example, a patient presents with pulmonary edema. flow distribution, which exclude overhydration or cardiac fail-
The lungs show no evidence of chronic lung disease, the ure, but the edema tends to be much more homogeneous
heart size is normal, the VPW is normal, there is no increase than usual, as opposed to the typically patchy distribution of
in PBV, and the distribution of blood flow appears normal, all capillary permeability edema, and has much less of an alveolar
indicating strongly that there is no overhydration and no
component. The patient’s lung compliance is not usually as
cardiac decompensation. This should, therefore, be a case of
low as the average adult respiratory distress syndrome case.
capillary permeability edema, but we find that the distribution
In such circumstances, one should suspect that there may be
of edema is atypical-it is neither peripheral, central, nor
an allergic basis for the edema-that the fluid is probably not
even, but has a bizarre appearance. In addition, we find that
proteinaceous and can clear quite rapidly and completely
there are peribronchial cuffs present (quite atypical for capil-
when the allergen (usually a drug) is identified and removed.
lary permeability). The features do not fit any of the classic
patterns described, and neurogenic pulmonary edema then Our study confirms that it is possible in a high proportion
becomes a consideration; the referring clinician should be of cases to identify correctly the cause of pulmonary edema
questioned regarding the possible occurrence of head trauma, by analysis of a given set of features on the chest radiograph.
intracranial hemorrhage, elevated cerebrospinal fluid pres- In many instances, this may eliminate the need for interven-
sure, etc. tional techniques and not infrequently will assist in the proper
Neurogenic edema is often accompanied radiologically by interpretation of wedge pressure recordings, which are not
an abrupt dilatation of the main pulmonary artery, reflecting invariably correct, and therefore, in the proper management
the huge rise in pulmonary artery and systemic pressures that of the patient.
892 MILNE ET AL. AJR:144, May 1985

failure. In: Hurst JW, ed. The heart, arteries and veins. New York:
McGraw-Hill, 1978:561-580
5. Ingram RH, Braunwald E. Pulmonary edema: Cardiogenic and
noncardiogenic forms. In: Braunwald E, ed. Heart disease. Phil-
adelphia: Saunders, 1980:71-589
6. Gray BA, Hyde RW, Hodges M, Vu PN. Alterations in lung volume
Downloaded from www.ajronline.org by 103.148.235.3 on 07/05/21 from IP address 103.148.235.3. Copyright ARRS. For personal use only; all rights reserved

and pulmonary function in relation to hemodynamic changes in


acute myocardial infarction. Circulation 1979;59: 551-559
7. Petty TL, Silvers GW, Paul GW, Standford RE. Abnormalities in
lung elastic properties and surfactant function in adult respiratory
distress syndrome. Chest 1979;75: 571-574
CT Scan 8. Fein A, Grossman RF, Jones JG, Goodman PC, Murray JF.
Evaluation of transthoracic electrical impedance in the diagnosis
of pulmonary edema. Circulation 1979;60: 1156-1160
9. Pedersen PC, Johnson CC, Durney CH, Bragg DG. Microwaves
reflection and transmission measurements for pulmonary diag-
nosis and monitoring. IEEE Trans Biomed Eng 1978;25:40-48
10. Gamsu G, Kauffman L, Swann SJ, Brito C. Absolute lung density
in experimental canine pulmonary edema. Invest Radiol
1979;1 4:261-268
11 Simon DS, Murray JF, Staub NC. Measurement
. of pulmonary
edema in intact dogs by transthoracic gamma-ray attenuation. J
AppI Physiol 1979;47: 1228-1233
12. Chinard FP. Estimation of extravascular lung water by indicator-
dilution techniques. Circ Res 1975;37 :137-145
13. Pistolesi M, Giuntini C. Assessment of extravascular lung water.
Radiol Clin North Am 1978;16:551-574
14. Lewis FR, Elings VB, Sturm JA. Bedside measurement of lung
water. J Surg Res 1979;27:250-261
15. Nobel WH, Kay JC, Maret KH, Caskanette G. Reappraisal of
PA Projection
extravascular lung thermal volume as a measure of pulmonary
edema. J App! Physiol 1980;48:120-129
16. Gonn AB, Kohler J, Denardo G. Noninvasive measurement of
pulmonary transvascular protein flux in normal man. J Clin Invest
1980;66:869-877
17. Sibbald WJ, Driedger AA, Moffat JD, Myers ML, Reid BA, Holli-
day RL. Pulmonary microvascular clearance of radiotracers in
human cardiac and non-cardiac pulmonary edema. J AppI Physiol
1981;50: 1337-1 347
18. Tatum JL, Strash AM, Sugerman HJ, Hirsch JI, Beachley MC,
‘:‘-
Greenfield U. Single isotope evaluation of pulmonary capillary
j.&.,’ ....z protein leak (ARDS model) using computerized gamma scintig-
raphy. Invest Radio! 1981;16:473-478
Fig. 16.-CT scan: Each lobule, segment, and lobe of lung, opacified in this 19. Carlson RW, Schaffer RC, Michaels SG, Weil MH. Pulmonary
diagram of CT scan by capillary permeability edema (cross-hatching), has its edema fluid: spectrum of features in 37 patients. Circulation
own periphery. Appearance of plain PA or AP chest film is caused by 1979;60:1 161-1169
superimposition of all these opacified areas. Note. because capillary permea-
bility edema cannot flow through interstitium, interlobular septa are free of 20. Fein A, Grossman RF, Jones JG, et al. The value of edema fluid
edema and show up as distinct, nonopacified bands on CT. In cardiac edema, protein measurements in patients with pulmonary edema. Am J
septa are filled with fluid and appear as opacified bands. PA projection: When Med 1979;67:32-38
densities of areas of edema are superimposed (arrows) from back to front as
21 . Anderson RR, Sibbald WJ, Holliday RL, Driedger AA, Lefcoe M,
they are in PA chest film, they appear much denser at periphery of radiograph.
Distribution of edema seen on CT differs, therefore, from that seen on plain Reid B. Documentation of pulmonary capillary permeability in
film. human adult respiratory distress syndrome (ARDS) secondary
to sepsis. Ann Rev Respir Dis 1979;1 19: 869-877
22. Lefcoe MS, Sibbald WJ, Holliday RL. Wedged balloon catheter
angiography in the critical care unit. Crit Care Med 1979;7 :449-
453
REFERENCES
23. Eaton RJ, Taxman RM, Avioli LV. Cardiovascular evaluation of
1. Murray JF. Circulation. In: The normal lung. Philadelphia: Saun- patients treated with PEEP. Arch Intern Med 1983;1 43:1958-
ders, 1976 1961
2. Staub NC. Lung biopsy in health and disease. In: Staub NC, ed. 24. Logue RB, Rogers JV, Gay BB. Subtle roentgenographic signs
Lung water and solute exchange. New York: Marcel Dekker, of left heart failure. Am Heart J 1963;65:464-473
1978 25. Harrison MO, Conte PJ, Heitzman ER. Radiological detection of
3. Staub NC. Pulmonary edema. Physiol Rev 1974;54:678-81 1 clinically occult cardiac failure following myocardial infarction. Br
4. Spann JF, Hurst JW. Etiology and clinical recognition of heart J Radio! 1971;44:265-272
AJR:144, May 1985 RADIOLOGIC DISTINCTION OF EDEMA 893

26. Milne ENC. Correlation of physiologic findings with chest roent- retention. I. Uremic lung-fluid lung on pathogenesis and therapy.
genology. Radio! C!in North Am 1973;1 1 :17-47 Acta MedScand 1953;146:159-163
27. Van de Water J, Sheh JM, O’Connor NE, Miller IT, Milne ENC. 53. Crosbie WA, Snowden 5, Parsons V. Changes
in lung capillary
Pulmonary extravascular water volume: measurement and sig- permeability in renal failure. Br Med J 1972;4:388-390
nificance in critically ill patients. J Trauma 197010:440-449 54. Gibson DG. Haemodynamic factors in the development of acute
28. Nobel WH, Siniewicz DJ. Radiological changes in controlled pulmonary oedema in renal failure. Lancet 1966;2: 1217-1 220
Downloaded from www.ajronline.org by 103.148.235.3 on 07/05/21 from IP address 103.148.235.3. Copyright ARRS. For personal use only; all rights reserved

hypervolemic pulmonary oedema in dogs. Can Anaesth Soc J 55. Staub NC. Pulmonary edema due to increased microvascular
1975;22: 171 -1 85 permeability to fluid and proteins. Circ Res 1978;43:43-151
29. Snashall PD, Keyes SJ, Morgan BM, et al. The radiographic 56. Maruyama Y, Little JB. Roentgen manifestations of traumatic
detection of acute pulmonary oedema: a comparison of radi- pulmonary fat embolism. Radiology 1962;79:945-952
ographic appearances, densitometry and lung water in dogs. Br 57. Berrigan TJ, Carsky EW, Heitzman ER. Fat embolism: roentgen-
J Radio! 1981;4:277-288 ographic pathologic correlation in 3 cases. AJR 1966;96:967-
30. Staub NC. The measurement of lung water content. J Microwave 971
Power 1983;1 8:259-263 58. Stem WZ, Spear PW, Jacobson HG. The roentgen findings in
31 . Baron MG. Radiological and angiographic examination of the acute heroin intoxication. AJR 1968;1 03:522-532
heart. In: Braunwald E, ed. Heart disease. Philadelphia: Saun- 59. Milne ENC, Pistolesi M, Miniati M, Giuntini C. The vascular pedicle
ders, 1980:147-197 of the heart and the vena azygos. I. The normal subject. Radio!-
32. Hinshaw CH, Murray JF. Diseases of the chest. Philadelphia: ogy 1984;152:-8
Saunders, 1980:629-652 60. Pistolesi M, Milne ENC, Miniati M, Giuntini C. The vascular pedicle
33. Staub NC, Hogg JC. Clinical measurement oflung water content. and the vena azygos. II. In cardiac failure. Radiology
Chest 1981;79:3-4 1984;1 52:9-17
34. Casaburi E, Wasserman K, Effros RM. Detection and measure- 61 . Milne ENC, Burnett K, Aufnchtig 0, McMiIlan J, Imray TJ. Eval-
ment of pulmonary edema. In: Staub NC, ed. Lung water and uating cardiac size on portable films (abstr). Invest Radio!
solute exchange. New York: Marcel Dekker, 1978:323-375 1982;17:52
35. Snashall PD, Hughes JMB. Lung water balance. Rev Physiol 62. Milne ENC. Physiologic interpretation
of the chest radiograph.
Biochem Pharmacol 1981;89:5-62 In: Margulis A, Gooding CA, eds. Diagnostic
radiology. San
36. Kerley P. Lung changes in acquired heart disease. AJR Francisco: University of California, 1980:201-222
1957;80: 256-263 63. Milne ENC. Pulmonary patterns in heart disease. In: Partridge
37. Chait A. Interstitial pulmonary edema. Circulation 1972;45: 1323- JA, ed. A Textbook of radiological diagnosis, vol 2, The cardio-
1330 vascular system. London: H. K. Lewis, 1985
38. Meszaros WT. Lung changes in left heart failure. Circulation 64. Friedman WF, Braunwald E. Alterations in regional pulmonary
1973;47: 859-871 blood flow in mitral disease studied by radioisotope scanning:
39. Giuntini C, Lewis ML, Sales Luis A, Harvey RM. A study of the simple non-traumatic technique for estimation of left atrial pres-
pulmonary blood volume in man by quantitative radiocardiogra- sure. Circulation 1966;34:363-376
phy. J Clin Invest 1963;42:1589-1605 65. Giuntini C, Manani M, Barsotti A, Fazio F, Santolicandro A.
40. Doniach I. Uremic edema of lungs. AJR 1947;58:620-628 Factors affecting regional pulmonary blood flow in left heart
41 . Kirkpatrick JA, Fleisher DS. Roentgen appearance of the chest valvular disease. Am J Med 1974;57:421 -436
in acute glomerulo-nephritis in children. J Pediatr 1964;64:492- 66. Schreiber 55, Bauman A, Yalow RS, Berson SA. Blood volume
694 alterations in congestive heart failure. J Clin Invest 1954;33: 578-
42. Mehbod H, Gutman E. Changes seen on chest films following 585
dialysis. Radiology 1971;1 00:41-44 67. Figueras J, Weil MH. Blood volume prior to and following treat-
43. Schwartz EE, Onesti G. The cardiopulmonary manifestations of ment of acute cardiogenic pulmonary edema. Circulation
uremia and renal transplantation. Radio! Clin North Am 1978;57:349-354
1972;1 0: 569-581 68. Milne ENC, Pistolesi M, Miniati M, Giuntini C. Assessing fluid
44. Dick DR, Zilak CJ. Acute respiratory distress in adults. Radiology balance from the plain chest film (abstr). Invest Radio!
1973;1 06:497-501 1984;1 9: 550
45. Joffe N. The adult respiratory distress syndrome. AJR 69. Morrison WJ, Wetherill S, Zyroff J. The acute pulmonary edema
1974;122:719-731 of heroin intoxication. Radiology 1970;97 :347-351
46. Ostendorf P, Birzle H, Vogel W, Mittermayer C. Pulmonary 70. Kangarboo H, Beachley MC, Ghahremani GG. The radiographic
radiographic abnormalities in shock. Radiology 1975;155:257- spectrum of pulmonary complications in burn victims. AJR
263 1977;1 28:441-445
47. Milne ENC. Chest radiology in the surgical patient. Surg Clin 71 . Staub NC, Nagano H, Pearce ML. Pulmonary edema in dogs,
North Am 1980;60: 1503-1518 especially the sequency of fluid accumulation in lungs. J App!
48. Pistolesi M, Miniati M, Ravelli V. Giuntini C. Injury versus hydro- Physiol 1967;22 :227-240
static lung edema: detection by chest x-ray. Ann NY Acad Sci 72. Staub NC. The pathogenesis of pulmonary edema. Prog Card!-
1982;384 :364-380 ovasc Dis 1980:23:53-80
49. McLoud 1, Barash PG. Ravin CE. PEEP: radiographic features 73. Goshy M, Lai-Fook SJ, Hyatt RE. Perivascular pressure meas-
and associated complications. 1977;129:209-213
AJR urements by wick-catheter technique in isolated dog lobes. J
50. Zimmerman JE, Goodman LR, Shahvari MBG. Effect of mechan- App! Physiol 1979;46:950-955
ical ventilation and positive end-expiratory pressure (PEEP) on 74. Inoue H, lnoue C, Hildebrandt J. Vascular and airway pressures
chest radiograph. AJR 1979;1 33:811-815 and interstitialedema affect peribronchial fluidpressure. J App!
51. Milne ENC. Some new concepts of pulmonary blood flow and Physiol 1980;48: 177-185
volume. Radiol Clin North Am 1978;16:515-536 75. Bhattacharya J, Gropper MA, Staub NC. Interstitial fluid pressure
52. AIwall N, Lunderquist A, Olsson 0. Studies on electrolyte-fluid gradient measured by micropuncture in excised dog lung. J App!
894 MILNE ET AL. AJR:144, May 1985

Physiol 1984:56:71-277 79. Matthay MA, Landolt CC, Bhattacharya J, Staub NC. Alveolar
76. Hedlund L, Effman E, Bates M, Putman C. The CT appearance fluid removal from the lungs of sheep (abstr). C!in Res
of early pulmonary edema (abstr). Invest Radiol 1981;1 6:391 1980;28:9A
77. Crandall ED, Staub NC, Goldberg HS, Effros RM. Recent devel-
80. Weibel ER. Morphometry of the human lung. New York: Ace-
opments in pulmonary edema. Ann Intern Med 1983;99:808-
822 dernic, 1963
Downloaded from www.ajronline.org by 103.148.235.3 on 07/05/21 from IP address 103.148.235.3. Copyright ARRS. For personal use only; all rights reserved

78. Comper WD, Laurent TC. Physiologic function of connective 81. Maldonado D. High altitude pulmonary edema. Radio! Clin North
tissue polysacchandes. Physiol Rev 1978:58:55-315 Am 1978;16:537-549

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