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JACC: CARDIOVASCULAR IMAGING

VOL. 3, NO. 6, 2010

2010 BY THE AMERICAN COLLEGE OF CARDIOLOGY FOUNDATION


PUBLISHED BY ELSEVIER INC.

ISSN 1936-878X/$36.00
DOI:10.1016/j.jcmg.2010.02.005

Detection of Pulmonary Congestion by Chest


Ultrasound in Dialysis Patients
Francesca Mallamaci, MD,* Francesco A. Benedetto, MD, Rocco Tripepi,
Stefania Rastelli, MD, Pietro Castellino, MD PROF., Giovanni Tripepi, STAT. DR.,
Eugenio Picano, MD PROF., Carmine Zoccali, MD PROF.*
Reggio Calabria, Catania, and Pisa, Italy

O B J E C T I V E S This study sought to investigate clinical and echocardiographic correlates of the lung

comets score.
B A C K G R O U N D Early detection of pulmonary congestion is a fundamental goal for the prevention

of congestive heart failure in high-risk patients.


M E T H O D S We undertook an inclusive survey by a validated ultrasound (US) technique in a

hemodialysis center to estimate the prevalence of pulmonary congestion and its reversibility after
dialysis in a population of 75 hemodialysis patients.
R E S U L T S Chest US examinations were successfully completed in all patients (N 75). Before
dialysis, 47 patients (63%) exhibited moderate to severe lung congestion. This alteration was commonly
observed in patients with heart failure but also in the majority of asymptomatic (32 of 56, 57%) and
normohydrated (19 of 38, 50%) patients. Lung water excess was unrelated with hydration status but it
was strongly associated with New York Heart Association functional class (p 0.0001), left ventricular
ejection fraction (r 0.55, p 0.001), early lling to early diastolic mitral annular velocity (r 0.48,
p 0.001), left atrial volume (r 0.39, p 0.001), and pulmonary pressure (r 0.36, p 0.002). Lung
water reduced after dialysis, but 23 patients (31%) still had pulmonary congestion of moderate to severe
degree. Lung water after dialysis maintained a strong association with left ventricular ejection fraction
(r 0.59, p 0.001), left atrial volume (r 0.30, p 0.01), and pulmonary pressure (r 0.32, p
0.006) denoting the critical role of cardiac performance in the control of this water compartment in
end-stage renal disease. In a multiple regression model including traditional and nontraditional risk
factors only left ventricular ejection fraction maintained an independent link with lung water excess
(beta 0.61, p 0.001). Repeatability studies of the chest US technique (Bland-Altman plots) showed
good interobserver and inter-US probes reproducibility.
C O N C L U S I O N S Pulmonary congestion is highly prevalent in symptomatic (New York Heart

Association functional class III to IV) and asymptomatic dialysis patients. Chest ultrasound is a reliable
technique that detects pulmonary congestion at a pre-clinical stage in end-stage renal disease. (J Am Coll
Cardiol Img 2010;3:586 94) 2010 by the American College of Cardiology Foundation

From the *Nephrology and Renal Transplantation Unit Ospedali Riuniti and Consiglio Nazionale delle Ricerche Institute of
Bio-Medicine, Clinical Epidemiology and Physiopathology of Renal Diseases and Hypertension, Reggio Calabria, Italy;
Cardiology Service, Morelli Hospital, Reggio Calabria, Italy; Internal Medicine and Nephrology, University of Catania,
Catania, Italy; and Institute of Clinical Physiology, CNR, Pisa, Italy. Supported by grants of the CNR (National Research
Council) and from Regione Calabria, Department of Health (Italy).
Manuscript received December 1, 2009; revised manuscript received February 17, 2010, accepted February 19, 2010.

Mallamaci et al.
Pulmonary Congestion in Dialysis

JACC: CARDIOVASCULAR IMAGING, VOL. 3, NO. 6, 2010


JUNE 2010:586 94

hronic volume expansion, either clinically


apparent or occult, is a pervasive complication in patients with end-stage renal
disease (ESRD) maintained on dialysis.
Even though the independent prognostic power of
volume overload remains scarcely defined in epidemiologic studies, recent findings in a large multiethnic
cohort of American patients documented that fluid
accumulation between dialysis is a powerful predictor
of death and cardiovascular complications in this
population (1). There has been a quest for methods
aimed at estimating body fluids volume and for
personalizing fluids removal in ESRD (2,3). The
main issue for the achievement of dry weight by
dialysis is that volume subtraction should be tailored
to the individual patients hemodynamic tolerance
taking into full account cardiac performance, which is
very often compromised in ESRD patients (4,5).
Extravascular lung water (LW) is a relatively
small but fundamental component of body fluids
volume (6,7). This component represents the water
content of the lung interstitium that is strictly
dependent on the filling pressure of the left ventricle (LV), that is, the hemodynamic parameter
considered as the golden standard for guiding fluids
therapy in critical care.
In recent years, the use of chest ultrasound (US)
to detect LW has received growing attention in
clinical research in intensive care patients (8) and in
patients with heart failure (9). In the presence of
excessive LW, the US beam is reflected by subpleural thickened interlobular septa, a low impedance
structure surrounded by air with a high acoustic
mismatch. This US reflection generates hyperechoic reverberation artifacts between thickened
septa and the overlying pleura that are defined as
lung comets (10). Lung comets represent the US
equivalent of Kerley B lines in standard chest
X-rays. These artifacts (Fig. 1) are easily detected
with standard US probes. Remarkably, lung comets
are strongly related to LV filling pressure (capillary
wedge pressure) and the measurement of LW by
US has been formally validated against a golden
standard technique such as the indicator thermodilution method in a series of patients submitted to
cardiac catheterization (11). A recent proof-ofconcept study aimed at testing the regression of
lung comets along with fluids removal was based
just on hemodialysis patients (12), and chest US is
increasingly applied to detect and monitor pulmonary congestion in patients with chronic heart
failure (9) and to grade disease severity in acute
respiratory distress syndrome/acute lung injury (13).

587

The aim of the present study is 3-fold: 1) to


estimate the feasibility of LW measurements by chest
US in hemodialysis patients and to determine the
prevalence of pulmonary congestion in these patients;
2) to investigate the relationship between LW, body
fluids volume status, and echocardiographic parameters of cardiac performance; and 3) to study the effect
of standard ultrafiltration dialysis on LW.
METHODS

The study protocol conformed to the Declaration of


Helsinki and was approved by the local ethics
committee. All patients provided informed consent.
Patients. Between May 8 and July 7, 2009, we
invited, to take part into the study, all patients
undergoing chronic hemodialysis treatment and
those who initiated hemodialysis during this period
in the dialysis unit of our department (n 78).
Seventy-five patients (49 men and 26
women) accepted and were enrolled. HeABBREVIATIONS
AND ACRONYMS
modialysis patients were being treated
thrice weekly with standard bicarbonate
BIA bioelectric impedance
dialysis by cuprophan or semisynthetic
analysis
membranes. Forty-six patients were habitE/E= early filling to early
ual smokers (17 13 cigarettes/day).
diastolic mitral annular velocity
Sixty patients were on treatment with
ESRD end-stage renal disease
erythropoietin. Forty-two patients were
Kt/V fractional urea clearance
being treated with various antihypertenLV left ventricle
sive drugs (26 on monotherapy with
LW lung water
angiotensin-converting enzyme inhibitors,
NYHA New York Heart
calcium channel blockers, beta-blockers,
Association
angiotensin II receptor blockers, and other
US ultrasound
antihypertensive drugs) and the remaining
16 patients were on double or triple therapy with various combinations of these drugs.
Patients were classified as symptomatic or asymptomatic on the basis of a slightly modified New
York Heart Association (NYHA) scale (14). Total
body water volume was estimated in each patient by
bioelectrical impedance analysis (BIA) by using a
standard apparatus (Akern BIA 101/S, Florence,
Italy) and the subjects nutritional and hydration
status was interpreted in relationship to normative
data in the Italian general population (15).
Lung comets detection and lung comets score. A
standard (3.0-MHz) echocardiography probe
(Toshiba Nemio XG, Toshiba, Tokyo, Japan) was
used for the detection of lung comets. Examinations were performed in the supine position. Scanning of the anterior and lateral chest was performed
on both sides of the chest, from the second to the
fourth (on the right side to the fifth) intercostal

588

Mallamaci et al.
Pulmonary Congestion in Dialysis

JACC: CARDIOVASCULAR IMAGING, VOL. 3, NO. 6, 2010


JUNE 2010:586 94

Figure 1. US of Normal Lung and Pulmonary Congestion


(Left) Normal lung ultrasound (US): the regular, parallel, horizontal hyperechogenic lines are due to the lung-wall interface. (Right) Pulmonary congestion: lung comets are hyperechogenic, coherent vertical bundles with narrow basis spreading from the transducer to the
further border of the screen.

spaces, at parasternal to mid-axillary lines, as previously described (8). Lung comets were recorded in
each intercostal space and were defined as a hyperechoic, coherent US bundle at narrow basis going
from the transducer to the limit of the screen (Fig.
1). These extended comets arise from the pleural
line and should be differentiated from short comets
artifacts that may exist in other regions. Lung
comets starting from the pleural line can be either
localized or scattered to the whole lung and be
present as isolated or multiple artifacts (with a
distance 7 mm between 2 artifacts). The sum of
lung comets produces a score reflecting the extent of
LW accumulation (0 being no detectable lung
comet). More details are available in a 2-min movie
on YouTube (16). On the basis of this score, we
grouped patients into 3 categories of increasingly
severe pulmonary congestion (mild: 14 comets;
moderate: 14 to 30 comets; severe: 30 comets) as
described in detail elsewhere (17). All measurements were made by an observer unaware of the
result of clinical and echocardiography data.
Echocardiography. Echocardiographic measurements were obtained in each patient before and
after dialysis by a standard echocardiography instrument (Toshiba Nemio XG). Details on the echo-

cardiography protocol followed in our unit were


previously described (18).
Reproducibility studies. The interobserver reproducibility of comets scoring was assessed in a set of 24
consecutive patients. One of 2 observers is an expert
echocardiography technician who received specific
training on chest US, and the second observer is a
nephrology trainee with introductory level experience in renal US who was trained by the technician
(in a 2-h practical session) to measure the lung score.
The reliability of comets score over time was investigated in a series of 10 patients who maintained stable
(1 kg) body weight over 2 to 4 weeks. To test the
agreement of comets scoring by different probes, these
measurements were recorded in random order with
the 3.5-mHz probe (a probe routinely applied for
renal sonography) and the standard echocardiography
(3.0-mHZ) probe in a series of 21 consecutive patients
and then read by a blind observer.
Statistical analysis. Data are expressed as mean
SD, median, and interquartile range, or as percent
frequency, as appropriate. Comparisons among
groups were made by p value for linear trend (1-way
analysis of variance or chi-square test). Among
patients, comparisons were made by paired t test
(normally distributed data) or by Wilcoxon signed

Mallamaci et al.
Pulmonary Congestion in Dialysis

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JUNE 2010:586 94

rank test (non-normally distributed data). Correlations between variables were investigated by Pearson product moment correlation coefficient (r),
point-biserial correlation coefficient, or by Spearman rank correlation coefficient (rho), as appropriate. The agreement between continuous or discrete
data was tested by the Bland-Altman method and
by the concordance correlation coefficient, whereas
that between categorical variables was tested by
kappa statistics. Independent correlates of lung
comets score were identified by multiple linear
regression analysis. Significant independent correlates of lung comets were identified by backward
elimination strategy (p out: 0.10). Data are expressed as standardized regression coefficient (beta)
and p value. All calculations were made using a
standard statistical package (SPSS for Windows,
version 9.0.1, Chicago, Illinois).
RESULTS

All eligible patents (n 78) but 3 (1 patient with


severe mental handicap, 2 patients that refused to
take part for logistic reasons) agreed to participate
in the study. Thus, 75 patients (96%) were actually
enrolled. The demographic and clinical characteristics of the study population are reported in Table 1.
Six patients had chronic obstructive pulmonary

disease, 1 patient had a previous diagnosis of


Wegener granulomatosis, and 46 were smokers.
Seventy-three patients were virtually anuric (24-h
diuresis, 0 to 250 ml/min), whereas the remaining
patients had a 24-h urine volume ranging from 550
to 750 ml/24 h. On average, pre-dialysis arterial
pressure was 138 25/71 12 mm Hg and
post-dialysis was 124 28/68 13 mm Hg.
Eleven patients (15%) had hypoalbuminemia (serum albumin: 3.6 g/dl) and 36 presented mild to
moderate pedal edema before dialysis. Nineteen
(25%) patients had a NYHA score 3.
Pre-dialysis BIA. On the basis of individuals plot in
the reactance/resistance nomogram, 24 patients
(32%) were classified as overhydrated, 38 (51%) as
at normal hydration status, and 13 (17%) as hypohydrated. Among patients with moderate to severe
heart failure (NYHA functional class III to IV, n
19), 15 (79%) were overhydrated by BIA.
Chest US. Chest US examinations were successfully
completed in all cases (feasibility 100%). No data
were rejected. The time needed for the chest US
varied between 3 and 6 min (average: 4 min). Lung
comets score significantly reduced (p 0.001) after
dialysis (Fig. 2). The mean and the median number
of pre-dialysis lung comets (lung comets score) were
33 and 18, respectively. Lung comets score was 14
in 28 cases, 14 to 30 in 26 cases, and 30 in 21

Table 1. Main Demographic, Somatometric Clinical, and Pre- and Post-Dialysis Hemodynamic Data of the Study Population
Pre-Dialysis Lung Comets Score

Age, yrs

<14 (n 28)

14-30 (n 26)

>30 (n 21)

p for Trend

r (p)

56 16

65 13

69 11

0.001

0.31 (0.008)

0.48

0.15 (0.21)

BMI, kg/m2

26.8 6.9

26.7 4.2

25.6 5.3

Male sex, %

64%

58%

76%

0.44

Smokers, %

50%

62%

76%

0.07

0.21 (0.08)

Diabetes (%)

21%

23%

24%

0.84

0.04 (0.71)

0.18 (0.12)

Patients with CV comorbidities, %

29%

48%

52%

0.09

0.15 (0.19)

Patients with NYHA functional classication 3, %

11%

23%

48%

0.004

0.25 (0.03)

Cholesterol, mg/dl

139 30

155 37

149 38

0.27

0.08 (0.51)

Systolic pressure, mm Hg

138 24

139 22

136 29

0.75

0.24 (0.04)
0.12 (0.30)

Diastolic pressure, mm Hg

74 15

70 8

70 12

0.32

Heart rate, beats/min

78 12

71 9

79 17

0.83

0.25 (0.03)

11.8 1.4

12.1 1.3

11.9 0.9

0.92

0.17 (0.14)

Hemoglobin, g/dl
Albumin, g/dl
Sodium, mEq/l

4.0 0.4
137 3

4.1 0.4
138 3

3.9 0.6
136 4

0.53

0.18 (0.13)

0.34

0.15 (0.21)
0.02 (0.86)

Potassium, mEq/l

5.2 0.6

5.4 0.7

5.5 0.7

0.25

Calcium, mg/dl

4.3 0.4

4.3 0.4

4.6 0.7

0.13

0.18 (0.13)

Phosphate, mg/dl

5.3 1.3

5.0 1.5

4.7 1.6

0.20

0.14 (0.26)

1.39 0.29

1.32 0.30

1.21 0.37

0.06

0.25 (0.04)

Kt/V

Data are expressed as mean SD or as percent frequency, as appropriate. Bold values are statistically signicant.
BMI body mass index; CV cardiovascular; Kt/V fractional urea clearance; NYHA New York Heart Association.

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Lung comets score, BIA hydration status classication,


and echocardiographic parameters. The lung comets

P<0.001

200

Lung Comets (n)

590

150

100

50

Pre-dialysis

Post-dialysis

Figure 2. Individuals Pre- and Post-Dialysis Lung Comets Score


Among patients, comparison was made by using the Wilcoxon
signed ranks test (see the Statistical Analysis section for details).

cases. Overall, 47 of 75 patients (63%) had moderate to severe pulmonary congestion (i.e., a lung
comets score 14) before dialysis. The score was
higher in patients with symptomatic heart failure
(NYHA functional class III to IV) than in patients
without symptoms of heart failure, but the vast
majority of asymptomatic patients (32 of 56, 57%)
had a score 14, indicating moderate to severe
pulmonary congestion. Patients with lung disease
(n 7) had a higher (median: 44, interquartile
range 21 to 56 vs. median: 17, interquartile range 12
to 30) score than those without (p 0.03).
On the basis of the pre-dialysis score, patients
were divided into 3 pre-specified categories denoting increasingly severe LW accumulation (17) (no
or mild: 14 comets, moderate: 14 to 30 comets,
severe: 30 comets) (Table 1). Patients in the most
severe category were older, more frequently smokers, with lower fractional urea clearance (Kt/V), and
with NYHA functional class III to IV heart failure
as compared to those in the other categories (Table
1). These associations were confirmed in correlation
analyses (Table 1, last column), which also showed
weak but significant relationships between lung
comets and pre-dialysis systolic pressure (inverse
association) and heart rate (direct association).

score in patients identified as overhydrated by BIA


(median: 20, interquartile range 13 to 57) did not
significantly differ (p 0.35) from that in patients
with normal hydration status (median: 17, interquartile range 17 to 22) or that in hypohydrated
patients (median: 15, interquartile range 7 to 45),
and as much as 50% of the 38 patients who were
normohydrated had a score indicating moderate to
severe pulmonary congestion. The score was closely
related to anatomical and functional echocardiographic parameters (Table 2). Indeed patients in the
third lung comets category (30 comets, severe
congestion) had higher left ventricular mass index,
left atrial volume, and left ventricular end-diastolic
volume (LVEDV) than those in other 3 categories.
Furthermore, patients in the third category displayed compromised LV systolic function as denoted by lower LV ejection fraction in comparison
to other groupings. Correlation analyses substantially confirmed these categorical associations (Table 2, last column) and also revealed highly significant relationships of pre-dialysis lung comets with
early left ventricular filling velocity (E), early filling
to early diastolic mitral annular velocity (E/E=)
ratio, pulmonary pressure, and LVEDV. The relationships between lung comets and LV ejection
fraction, E/E= ratio, and left atrial volume were the
strongest among those considered in this study
(Fig. 3).
In a multiple regression model including standard clinical correlates (p 0.10) of lung comets
score (age, smoking, Kt/V, systolic pressure and
heart rate, and NYHA functional classification) as
well as anatomical (LV mass index) and functional
(ejection fraction, left atrial volume, pulmonary
pressure, and E/E= ratio) echocardiographic parameters of the left ventricle, results show only LV
ejection fraction to be an independent correlate of
the pre-dialysis score (beta 0.61, p 0.001).
Forcing serum albumin into the model did not
materially modify the link of the lung comets score
with LV ejection fraction.
Effect of dialysis on hydration status by BIA and on
lung comets. Body weight reduced from 66.7

18.0 kg pre-dialysis to 64.4 17.4 kg after dialysis


(3.4%, p 0.001). After dialysis, 7 out 24 patients
(29%) moved from the overhydration to the normohydration or hypohydration area. The proportion of patients with moderate to severe pulmonary
congestion fell from 47 (63%) to 23 (31%). The
association between the comets score and hydration

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Pulmonary Congestion in Dialysis

JACC: CARDIOVASCULAR IMAGING, VOL. 3, NO. 6, 2010


JUNE 2010:586 94

Table 2. Echocardiographic Data of the Study Population


Pre-Dialysis Lung Comets Score
Pre-Dialysis Echocardiographic Data

1430

<14

>30

p for Trend

r (p)

71 20

77 17

85 22

0.02

Left ventricular end-diastolic volume, ml

116 35

108 33

126 41

0.39

0.30 (0.01)

Left atrial volume, ml/m2.7

12.3 3.6

14.5 3.2

16.0 4.5

0.001

0.39 (0.001)

Early left ventricular lling velocity, cm/s

0.74 0.21

0.77 0.28

0.81 0.28

0.37

0.31 (0.008)

7.6 1.6

8.4 3.3

10.9 5.6

0.005

0.48 (<0.001)

LVMI, g/m

2.7

E/E= ratio

0.28 (0.01)

Ejection fraction, %

62 4

59 6

49 12

<0.001

0.55 (<0.001)

Pulmonary pressure, mm Hg

19 12

18 14

26 17

0.10

0.36 (0.002)

Data are expressed as mean SD or as percent frequency, as appropriate. Bold values are statistically signicant.
E/E= early lling to early diastolic mitral annular velocity; LVMI left ventricular mass index.

status by BIA improved after dialysis: among patients who were normohydrated after dialysis (n
25) only 4 (16%) had a score 14. Importantly
there was a high correlation between pre-dialysis
lung comets and the reduction in this score after
dialysis (Fig. 3). LVEDV fell from 116 37 ml to
103 32 ml after dialysis, as did left atrial volume
(from 14.1 4.0 ml/m2.7 to 12.6 3.6 ml/m2.7)
whereas LV ejection fraction remained unmodified
(57.4 9.3% vs. 57.4 9.5 %), denoting improved

LV performance. The decrease in lung comets after


dialysis was also strongly related with pre-dialysis
LV ejection fraction (r 0.55, p 0.001),
pre-dialysis E/E= ratio (r 0.38, p 0.001),
pre-dialysis left atrial volume (r 0.35, p 0.003),
pre-dialysis LVEDV (r 0.32, p 0.006), NYHA
functional class (r 0.32, p 0.005), pre-dialysis
LV end-diastolic diameter (r 0.31, p 0.007),
pre-dialysis LV mass index (r 0.29, p 0.01),
pre-dialysis pulmonary pressure (r 0.23, p

Pre-post Dialysis Changes


in Lung Comets Score

LVEF (%)

-20

rho = -0.55, P<0.001


rho = -0.59, P<0.001

80

70

20

60

40

rho = -0.85
P<0.001

60

50

80

40

100

30

120

20

140

10
0

20 40 60 80 100 120 140 160 180 200

50

Pre-dialysis Lung Comets Score

LAV (mL/m2.7)

E/E ratio
30
25

25

20

20

15

15

10

10

150

200

Pulmonary Pressure (mm Hg)

30

r = 0.48, P<0.001
r = 0.26, P = 0.04

100

Lung Comets (n)

70

r = 0.39, P = 0.001
r = 0.35, P = 0.01

r = 0.36, P = 0.002
r = 0.35, P = 0.003

60
50
40
30

50

100

150

Lung Comets (n)

200

20
10
0
0

50

100

150

Lung Comets (n)

200

50

100

150

200

Lung Comets (n)

Figure 3. Correlation Analyses of Pre- and Post-Dialysis Lung Comets Scores


Relationship between pre-dialysis comets score and pre-/post-dialysis change in the same score and pre- (pink circles) and post-dialysis
(green circles) relationships of the lung comets score with left ventricular ejection fraction (LVEF), E/E= ratio, left atrial volume (LAV), and
pulmonary pressure. Solid lines indicate pre-dialysis regression lines and dashed lines indicate post-dialysis regression lines. Data are
expressed as Pearson product moment correlation coefcient (r) or Spearman rank correlation coefcient (rho), as appropriate. E/E=
early lling to early diastolic mitral annular velocity.

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0.05); however, it was largely independent of the


volume of fluids removed across dialysis or changes
in systolic and diastolic pressures or serum albumin
(p NS). Notably the strength of the association
between the post-dialysis lung comets score and LV
ejection fraction (r 0.59, p 0.001), left atrial
volume (r 0.30, p 0.01) and pulmonary
pressure (r 0.35, p 0.003) was of a degree
similar to that observed before dialysis (Fig. 3). In
the 7 patients with pre-existing pulmonary disease,
the decrease in lung comet score (from 44 [median]
to 18, 59%) did not significantly differ (p 0.09)
from that in patients without pulmonary disease
(from 17 to 9, 47%).
Reproducibility studies. The reproducibility of the
lung comets score over time in 10 stable patients
who maintained a pre-dialysis body weight within
1 kg of the initial study was good in that the
difference between the 2 measurements was always
less than 2 SD of the average measurement (concordance index 0.83, 95% confidence interval:
0.60 to 0.93) (Fig. 4). The agreement between the
expert and the naive observer was quite satisfactory:
in over 24 independent measurements, only in 2

cases did the between-observer difference exceed 2


SD, and in 1 of these cases (very high score), the
difference did not modify the categorization of
the severity of pulmonary congestion (severe in
both cases) (Fig. 4). Equally good was the reproducibility of the comets score as measured with
the echocardiography probe (3.0 mHz) and the
standard renal probe (3.5 mHz) in that just in 1
case did the interprobe difference exceed 2 SD
(Fig. 4).
DISCUSSION

Chest US is a simple, easy to perform, and quick


technique that provides reproducible estimates of
LW in hemodialysis patients. By this technique,
LW is strikingly increased in the vast majority of
symptomatic and asymptomatic ESRD patients
and appears strongly associated with altered LV
performance but scarcely related with hydration
status before dialysis. Standard ultrafiltration dialysis markedly reduces LW and improves LV performance but fails to normalize this parameter in most
cases. Overall findings in this study indicate that

Reproducibility in Stable Patients


50
[Lung Comets (1st meas)
- Lung Comets (2nd meas)]

40

+2 Standard Deviations (SD)

30
20
Average

10
0
-10

-2 SD

-20
-30
-40
0
20
40
60
80
100
120
[Lung Comets (1st meas) + Lung Comets (2nd meas)]/2

Inter-observers Agreement

Inter-probes Agreement

60

40

+2 SD

20
Average

-20
Concordance index=0.96
95% CI: 0.90-0.98

-2 SD

-40

[Lung Comets (3.0 MHz)


- Lung Comets (3.5 MHz)]

13
[Lung Comets (1st Obs)
- Lung Comets (2nd Obs)]

592

9
+2 SD

Average

1
-3

-2 SD

-7
-11

Concordance index=0.99
95% CI: 0.98-1.00

-15
0
50
100
150
200
[Lung Comets (1st Obs) + Lung Comets (2nd Obs)]/2

0
20
40
60
80
100
[Lung Comets (3.0 MHz) + Lung Comets (3.5 MHz)]/2

Figure 4. Reproducibility Studies of Lung Comets Scores


Reproducibility studies of the lung comets score over time (upper graph) in 10 stable patients who maintained a pre-dialysis body
weight within 1 kg of the initial study. Interobserver and interprobe agreements were ascertained in a series of 24 independent measurements (bottom graphs). All graphs are Bland-Altman plots (see the Statistical Analysis section for details). Abbreviations as in Figure 3.

Mallamaci et al.
Pulmonary Congestion in Dialysis

JACC: CARDIOVASCULAR IMAGING, VOL. 3, NO. 6, 2010


JUNE 2010:586 94

chest US gives reliable information that can be


potentially useful for complementing the characterization of cardiac performance and body fluids
status in hemodialysis patients.
Fluids overload and pulmonary congestion in ESRD
and in heart failure. Accumulation of fluids in the

lung is the most concerning consequence of fluids


overload and pulmonary congestion, and congestive
heart failure is a notorious, frequent complication in
ESRD (19). The risk of pulmonary congestion due
to fluids overload is particularly high in the presence
of compromised LV function (20). In these cases,
even a minor degree of fluids excess may translate
into clinical symptoms of pulmonary congestion.
The joint effect of fluids excess and LV dysfunction
on pulmonary water is of paramount importance in
ESRD because about 30% of patients entering
chronic dialysis display frank symptoms of heart
failure (21) and because as much as 48% of asymptomatic patients stabilized on dialysis have compromised LV function (5). Pulmonary capillary wedge
pressure, which reflects LV filling pressure, is the
driving force determining fluids extravasation into
the lungs, a phenomenon that only occurs after
substantial fluids accumulation in patients without
heart disease (22) but even in the absence of fluids
retention in patients with LV failure (23).
LW and LV function in ESRD. Patients with ESRD
accumulate water in the lungs as their extracellular
volume expands (24,25). We found that chest US, a
technique with a very short learning curve that can
be performed by standard equipment, provides reproducible estimates with good interobserver and
interprobe agreement. Importantly, our observations
in an inclusive population of ESRD patients, comprising 19 (25%) with NYHA functional class III to
IV heart failure, show that LW before dialysis is
highly dependent on LV function but largely independent of total body water. The close, inverse association between LW and ejection fraction, both before
and after dialysis, clearly points to LV dysfunction as
a main driver of pulmonary congestion.
Extending observations in patients with heart failure (10), our study provides evidence that chest US
captures pulmonary congestion at a pre-clinical stage

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Chest US is a reliable technique for estimating LW


in dialysis patients. Subclinical pulmonary congestion is prevalent in asymptomatic and normohydrated dialysis patients. Chest US may prove useful
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Acknowledgments

Maurizio Ciccarelli, Pietro Finocchiaro, and Vincenzo Panuccio were responsible together with
Francesca Mallamaci for the clinical management
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The authors are grateful to the nurse personnel for
the help given in this study.
Reprint requests and correspondence: Dr. Carmine Zoccali, Nefrologia e CNR, Ospedali Riuniti, c/o Euroline di
Ascrizzi Vincenzo, Via Vallone Petrara n. 55-57, 89124
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Key Words: dialysis y lung


comets y pulmonary congestion.

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