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Am J Respir Crit Care Med Vol 158. pp 16441655, 1998Internet add ress: www.atsjournals.org

A Computed Tomography Scan Assessment of RegionalLung Volume in Acute Lung Injury

LOUIS PUYBASSET, PHILIPPE CLUZEL, NAN CHAO, ARTHUR S. SLUTSKY, PIERRE CORIAT,

JEAN-JACQUES ROUBY, and th e CT Scan ARDS Study Group

Unit de Ranimation Chirurgicale, Department of Anesthesiology and Department of Radiology (Thoracic Division),

La Piti-Salptrire Hospital, University of Paris VI, Paris, France; and Department of Medicine and Pathology,

Mount Sinai Hospital, University of Toronto, Toronto, Canada

The lobar and cep halocaudal distribution of ae rated and nonaerate d lung and o f PEEP-induced alveo-

lar recruitment is unknown in acute lung injury (ALI). Dimensions of the lungs and volumes of aer-

ated and nonaerated parts of each pulmonary lobe were measured using a computerized tomo-

graph ic quantitative analysis and co mp ared b etwee n 21 patients with ALI and 1 0 he althy volunteers.

Distribution of PEEP-induced alveolar recruitme nt along the anterop osterior and cep halocaudal axis

and influence of the resting volume of nonaerated lower lobes were also assessed. Anteroposterior

and transverse dimensions of the lungs of the patients were similar to those of healthy volunteers,

whereas cephalocaudal dimensions were reduce d by more than 15% . Total lung volume ( aerated

plus nonaerated lung) was reduced by 27% . Volumes of upper and lower lobe s were 99 and 48% of

normal values. In addition to an anteroposterior gradient in the distribution of aerated and nonaer-ated areas, a cephalocaudal gradient was also observed. Nonaerated areas were predominantly

found in juxtadiaphragmatic regions. PEEP-induced alveolar recruitment was more pronounced in

nonde pen dent th an in depe ndent reg ions and in ceph alad than in caudal reg ions. A significant corre-

lation b etwee n resting volume o f nonae rated lower lobe s and regional PEEP-induced alveolar recruit-

ment was observed. In ALI, loss of lung volume involves predominantly lower lobes. The thorax

shortens along its cephalocaudal axis. PEEP-induced alveolar recruitment predo minates in no ndep en-

dent and cephalad lung regions and is inversely correlated with the resting volume of nonaerated

lung. Puybasset L, Cluzel P, Chao N, Slutsky AS, Coriat P, Rouby J-J, and the CT Scan ARDS Study

Group. A computed tomography scan assessment of regional lung volume in acute lung in-

jury.

AM J RESPIR CRIT CARE MED 1998;158:16441655.

Lo ss of aera ted lung volume is a characteristic feature of acutelung injury (ALI) and is commonly observed after major tho-racic and abdominal surgical procedures. Reduction in lungvolume is generally a ssessed by measuring FRC , using gas di-lution techniques such as nitrogen (1) or sulfur hexafluoride(2, 3) washout and open- and closed-circuit helium dilution

techniques (1, 4). These methods have t he ad vanta ge of beingnoninvasive, allowing bedside and repeated measurements.H owever, they a re not a lway s reproducible (1, 2, 5) and do notprovide any measurement of the volume of nonaerated lung.Furthermore, there are some important limitations common

to all these techniques when applied to patients with ALI: (

1

)the diseased lung is characterized by the presence of poorlyaerated areas where the gas mixing is problematic, (

2

) disten-tion of previously aerated regions cannot be distinguishedfrom true alveolar recruitment when FRC increases after pos-itive end-expiratory pressure (PEEP), and (

3

) regional d istri-bution of aerated and nonaerated lung volumes and of P EE P-

induced alveolar recruitment cannot be a ssessed.Chest computerized tomography (CT scan) is a technique

that can overcome some of the limitations of these methods.B y measuring lung densities, well-aera ted regions can be ea s-ily differentiated from poorly and nonaerated lung regions. Inpatients critically ill with ALI, it has been demonstrated thatlung hyperdensities predominat e in the dependent regions (3,6, 7). The superimposed hydrostatic pressure resulting fromthe edematous lung along an anteroposterior axis has beenproposed to be a likely explanation for this regional distribu-tion gradient (8, 9). Similarly, PEEP-induced alveolar recruit-ment has been shown to depend upon an anteroposterior gra-dient, the mo st dependent lung regions being less likely to b e

(

Received in original form February 3, 19 98 and in revised form July 6, 1 998

)

The following members of the CT Scan ARDS Study Group participated in thisstudy: T. E. Stewart, M.D., Ewart Angus ICU, Wellesley Hospital, Toronto Canada;P. Grenier, M.D., and S. Zaim, M.D., Department of Radiology, La Piti-

Salptrire Hospital, Paris, France; L. Gallart, M.D., and M. Puig, M.D., ServeidAnestesiologia, Hospital Universitari del Mar, Barcelona, Spain; G. S. Umama-heswara Rao, M.D., Department of Anesthesia, National Institute of MentalHealth and Neurosciences, Bengalore, India; J. Richecoeur, Ranimation Mdi-cale Polyvalente, Pontoise, France; S. Vieira, M.D., Hospital de Clinicas de PortoAllegre, UFRGS, Brazil; and Q. Lu, M.D., Unit de Ranimation Chirurgicale,Hpital de La Piti-Salptrire, Paris, France.

Presented in part at the annual meeting of the European Society of Anesthesiol-ogy, London, United Kingdom, June 1996 and at the Annual Meeting of theAmerican Thoracic Society, New Orleans, Louisiana, May 1996.

Correspondence and requests for reprints should be addressed to Dr. L. Puybas-set, Surgical Intensive Care Unit, Department of Anesthesiology, La Piti-Sal-ptire Hospital, 47-83, Boulevard de lHpital, 75013 Paris, France.

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TABLE 1

CLINICAL CHARACTERISTICS OF THE PATIENTS

Patient

No.

Age

(

yr

) Sex Cause of ALI

Surgical

Incision Outcome SAPS ASA LISS

Ventilation

Duration

(

d

)

ICU

Duration

(

d

)

1 70 M BPN NTNA S 19 2 1.5 22 18

2 72 F BPN NTNA D 16 2 3.75 102 102

3 35 M PC THO/ABD S 10 1 2.25 25 29

4 69 M BPN THO S 13 3 3.0 37 34

5 50 F AP NTNA S 11 2 2.25 39 43

6 46 M BPN ABD D 18 3 1.7 26 25

7 38 M Pancreatitis NTNA D 19 2 3.5 28 15

8 44 F BPN NTNA D 8 1 3.0 37 36

9 71 M BPN THO/ABD S 14 3 3.25 36 44

10 66 M BPN NTNA D 20 2 3.25 24 16

11 45 M BPN THO S 14 2 2.5 26 33

12 34 M BPN ABD S 15 1 2.5 76 107

13 70 M BPN NTNA S 11 3 2.0 20 20

14 43 M BPN NTNA S 13 1 1.25 69 129

15 64 M BPN NTNA S 16 2 2.25 48 48

16 69 F SS ABD D 12 3 3.0 36 31

17 66 M BPN ABD S 18 3 2.0 13 18

18 81 M AP NTNA S 15 3 2.75 32 35

19 20 M PC NTNA S 10 1 3.25 31 22

20 61 M BPN NTNA D 10 3 3.5 14 7

21 40 F SS ABD D 14 1 3.0 13 11

Mean 14.1 2.1 2.6 36 39SD 3.4 0.8 0.7 22 33

Definition of abbreviations

: ABD abdominal; ALI acute lung injury; AP

aspiration pneumonia; ASA

Score of the American Societyof Anesthesiology; BPN

nosocomial pneumonia; D

deceased; LISS

lung injury severity score; NTNA

nonthoracic and nonabdomi-nal; PC

pulmonary contusion; S

survived; SAPS simplified acute physiological score; SS

septic shock; THO

thoracic.

TABLE 2

RESPIRATORY CHARACTERISTICS OF THE PATIENTS

Patient

No.

% Well

Aerated

% Poorly

Aerated % Nonaerated

Cst

(

ml/cm H

2

O

)

Pop

(

cm H

2

O

)

Pa

O2

(

mm Hg

)

Ppa

(

mm Hg

)

DA

/V

T

(

%

)

1 77 2 21 77 5 159 22 33

2 1 68 31 43 6 197 24 ND

3 23 47 30 36 ABS 81 27 18

4 82 11 7 50 6 104 43 35

5 48 20 33 42 6 69 21 35

6 60 22 19 38 4 90 53 ND

7 0 66 34 32 6 49 17 ND

8 35 37 27 37 7 77 25 36

9 67 9 24 64 3 58 39 ND

10 17 47 36 29 7 39 36 44

11 29 44 27 40 5 249 22 ND12 8 55 37 35 10 115 31 50

13 0 75 25 60 ABS 111 41 33

14 59 16 26 54 3 82 18 27

15 16 34 50 28 ABS 73 49 32

16 2 51 47 44 ABS 79 33 47

17 31 47 21 87 5 247 22 42

18 36 17 47 63 4 125 34 42

19 9 31 59 34 9 76 41 51

20 38 7 54 30 6 59 45 33

21 8 60 32 22 10 50 35 67

Mean 31 36 33 45 6 104 32 39

SD 26 22 13 17 2 60 11 11

Definition of abbreviations

: ABS

absent; Cst

quasi-static compliance; Pop

opening pressure determined after subtraction of intrin-sic-PEEP; Ppa

mean pulmonary artery pressure; DA

/V

T

alveolar dead space to tidal volume.

V

V

recruited by PEEP than the nondependent lung regions (10).B ecause these different studies were performed using a lim-ited number of CT sections (one to three), measurements ofthe volume of the entire lung and of ea ch pulmonary lob e andassessment of the cephalocaudal distribution of lung consoli-dat ions could not be performed. The present study wa s under-

taken to quantify lung volume loss and to assess its lobar dis-tribution in patients with ALI. In addition, PEEP-inducedalveolar recruitment and its anteroposterior and cephalocau-dal distribution were studied after obtaining contiguous tho-racic CT sections from the apex to the diaphragm with andwithout PE EP .

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METHODS

Patients

Twenty-one consecutive hypoxemic patients with ALI diagnosed onor after admission to the Surgical Intensive Care Unit of La Piti-Salptrire Hospital in Paris (D epartment of Anesthesiology) wereincluded in a prospective study during the first 10 d o f their a cute re-spirato ry disease. All of them were transported to the D epartment ofRadiology and underwent a thoracic CT scan after informed consenthad been obtained from their next of kin. Sixteen patients had theirCT scans performed as they were enrolled in prospective studies oninhaled NO . The description of the C T scan procedure and of t he risksof the tra nsportation were clearly mentioned in the document accom-panying the inform consent that wa s signed by the fa milies. The clini-cal and ra diologic characteristics of these patients have been reportedin previously published articles (1113). For the five remaining pa-tients who w ere not included in studies on inhaled NO, complete ex-planations about the CT scan procedures were given to the families,and inform consent wa s obtained fro m all of them b efore inclusion in

the study. Inclusion criteria w ere: (

1

) bilateral opacities on a bedside

chest radiograph, (

2

) Pa

O

2

250 mm Hg at an F

IO 2

of 1.0 and zeroend-expiratory pressure (ZEEP). Exclusion criteria were (

1

) cardio-genic pulmonary edema defined as a pulmonary capillary w edge pres-sure

18 mm H g and a left ventricular ejection fraction

50% as es-timated by a bedside transesophageal echocardiography, and (

2

) thepresence of a bronchopleural fistula.

All the patients were sedated and paralyzed with a continuous in-travenous infusion of fentanyl 250

g/h, flunit ra zepa m 1 mg/h, and ve -curonium 4 mg/h and vent ilated using controlled mecha nical ventila -tion (Csar V entilator; Taema, A ntony, France). An inspirato ry timeof 30% and an F

IO2

of 1 were maintained throughout the study period.All patients were monitored using a fiberoptic thermodilution pulmo-nary artery catheter (Baxter H ealthcare Co., Irvine, CA) a nd a radialor femoral arterial catheter.

High Resolution a nd S piral Thoracic CT Scan

As previously described (1113), lung scanning was performed fromthe apex to the diaphragm using a Tomoscan SR 7000 (Philips, Eind-hoven, The Netherlands). All images were observed and photo-graphed at a window w idth of 1,600 HU and a level of

700 HU . Anintravenous injection of 60 ml of cont rast ma terial w as ad ministeredto ea ch patient to differentiate pleural fluid collections from consoli-

dat ed lung parenchyma. E valuation included thin-section C T and spi-ral CT in all patients. The thin-section CT examination consisted of aseries of sections 1.5 mm thick with 20-mm intersection spacing se-lected by mea ns of a thoracic scout view during a 25-s period of a pnea,the paralyzed pa tient being disconnected from the ventilator (pulmo-nary volume equal to apneic FRC, ZEEP). For spiral CT, contiguousaxial sections 10 mm thick were reconstructed from the volumetricdata obtained during a 15-s apnea. A PEEP of 10 cm H

2

O was thenapplied for 15 min during controlled mechanical ventilation. The sameCT scan prot ocol (thin-section and spiral CT) was repeated at an end-expiratory pressure of 10 cm H

2

O by clamping the endotracheal tubeconnector at end-expiration (pulmonary volume equal to FRC afterPEEP administration). Airway pressure was continuously monitoredto ensure that a P EE P value of 10 cm H

2

O w as maintained during theCT acquisition. Mechanical ventilation was provided using an Osirisventilator (Taema) specifically designed for transportation of criti-cally ill patients and delivering 100% oxygen. Cardiovascular moni-toring was performed using a Propaq 104 EL monitor (Protocol Sys-tem, Beaverton, OR), allowing the continuous monitoring of pulseoximetry, systemic arterial pressure, and electrocardiogram. All theCT scans were performed with t he patients in t he supine position.

A spiral thoracic CT scan consisting of contiguous axial sections 10mm thick was also performed at end-expiration in 10 spontaneouslybreathing hea lthy volunteers.

Volumetric Analysis of the Thoracic CT Scan

The aim of this analysis was to measure the volumes (gas plus tissue)and the anteroposterior and cephalocaudal distribution of the differ-ent lung zonesaerated, poorly aerated, and nonaeratedin ZEEPand PEEP conditions. Lung parenchyma was manually delineated by

Figur e 1. From the upperto the lowerpart of the figure: volumes

of upper and lower lobes and cephalocaudal dimensions of rightand left lungs obtained from the 10 healthy volunteers; volumes ofupper and lower lobes and cephalocaudal dimensions of right andleft lungs obtained from the 21 patients with acute lung injury;and volumes of normally and poorly aerated areas of upper andlower lobes obtained from the 21 patients with acute lung injury.All volumes and dimensions were measured at zero end-expiratorypressure. Each lung is drawn in profile. The oblique fissura is repre-sented by the continuous lineand the horizontal fissura is repre-sented by the dashed line.

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one of the investigators (P.C .) after marking mediastinal structures andpleural effusion. Upper and low er lobes were delineated a fter fissureshad been precisely identified on the thin sections. A specially de-signed transparent grid that had a between-line distance fitted to the1-cm scale of the CT scan image was applied to each CT section fromthe a pical to the diaphragma tic sections. As the thickness of each vol-umetric CT section was 1 cm and ea ch square of the grid represented

a surface of lung parenchyma of 1 cm

2

, each square represented a lungvolume of 1 cm

3

. The first line of the grid was applied to each CT sec-tion in order t o precisely fit the a nterior margin of lung parenchyma.The total number of squares was determined for each line from theanterior to the posterior lung region. In order to measure the respec-tive lung volumes of aerated , poorly aerated, and nona erated lung ar-eas, the radiologic density of each square of the grid was visually as-sessed by comparing its aspect to the gray scale of the CT scan andclassified in one of the three categories proposed by G attinoni and col-leagues (6): areas corresponding to a density between

1,000 and

500 HU were considered as well aerated, areas corresponding to adensity between

500 and

100 HU were considered as poorly aer-ated, and areas corresponding to a density between

100 and

100HU were considered as nonaera ted. This analysis was performed sep-ara tely for upper and lower lob es. Because the right middle lobe couldnot easily be distinguished from the right upper lobe, it was consid-

ered as a pa rt of the right upper lobe for the regional volume analysis.The amount of pleural fluid wa s also determined. As t he volumetricanalysis was performed in ZEEP and PEEP conditions, changes inlung volumes induced by PEEP could be precisely measured. PEEP-induced alveolar recruitment w as calculated as the difference betw eenthe volume of nonaerated tissue in ZE EP minus the volume of nonaer-ated tissue in PEEP. Percentage of PEEP-induced alveolar recruit-ment wa s calculated a s the volume recruited divided by the volume ofnonaerat ed lung. A patient was arbitrarily defined as a recruiter ifPEEP reduced the volume of nonaerated tissue by more than 10%;otherwise the patient wa s considered a nonrecruiter.

The mean of t he individual difference between t wo o bservers was3

158 ml for total lung volume and 2

11 ml for pleural effusionvolume measurements (n

8). Intraobserver differences were 15

75 and 7

9 ml, respectively (n

6).

Figur e 2. Sagittal reconstructions of the right lung (mediastinal windows) obtained from the contiguous CT sections in one patient withacute lung injury (left side) and one healthy volunteer (right side). The centimetric scale on the right side has a height of 20 cm.

The cephalocaudal dimension of each lung wa s determined as thenumber of sections 1 cm thick present betw een the lung apex and thedome of the diaphragma tic cupola. Transverse and ant eroposterior di-mensions were determined a t the level of the tra cheal carina using thelength scale of t he CT scan. For each pat ient, a sagittal section of theright lung was reconstructed from contiguous CT sections. Recon-struction was performed at the maximal convexity of the right dia-

phragmatic cupola analyzed on the front al scout view.Volumes of right and left upper and lower lobes and cephalocau-dal, transverse, and anteroposterior distances were also measured inthe 10 healthy volunteers at end-expiration. These measurementswere performed to determine normal values of the lung dimensionsand volumes.

Hemodynamic Measureme nts

Hemodynamic and respiratory variables in ZEEP and 15 min afteradministration of PE EP were measured within the 24 h before or afterthe CT scan in patients with ALI. Systemic and pulmonary arterialpressures were measured using the arterial ca nnula and the fiberopticpulmonary a rtery catheter connected to t wo calibrat ed pressure trans-ducers (PX-1X2; Baxter SA, Maurepas, France) positioned at themidaxillary line and recorded along with the EK G and trachea l pres-

sure on a G ould E S 1000 recorder (G ould Instruments, Ba llainvilliers,France). All pressures were measured a t end-expiration. C ardiac o ut-put was measured using the thermodilution technique and a bedsidecomputer, which allowed the record ing of ea ch thermodilution curve(Explorer; Ba xter Hea lthcare). Systemic and pulmonary a rterial bloodsamples were simultaneously withdrawn within 1 min after the mea-

surements of cardiac output. Arterial pH, P a

O

2

, P v

O

2

, and Pa

CO

2

weremeasured using an IL B G E b lood gas analyzer (InstrumentationLaboratories, Paris, France). Hemoglobin concentration, and methe-moglobin concentration, and arterial and mixed venous oxygen sat-uration (Sa

O

2

and Sv

O

2

) were measured using a calibrated OSM3hemoximeter (Radiometer Copenhagen, Neuilly-Plaisance, France).Standard formulas were used to calculate cardiac index, true pulmo-

nary shunt (

S

/

T

), oxygen delivery (

O2

), and oxygen consumption(

O2

).Q.

Q.

D.

V

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Respiratory Measurements

Expired C O

2

was measured using a nonaspirative calibrated 47210Ainfrared capnometer (Hewlett-Packard, Andover, MA) positionedbetween the proximal end of the endot racheal tube and t he Y-piece ofthe ventilator a nd recorded on t he G ould ES 1000. After simulta-neously withdrawing an arterial blood sample, the ratio of alveolardead space (

D A

) to t idal volume (V

T

) was calculated as:

(1)

where P

ETCO 2

is end tidal C O

2

measured at t he plateau of t he expiredC O

2

curve.R espiratory volume-pressure curves were ob tained using t he gross

syringe technique (14) and opening pressure (Pop) was visually deter-mined. Quasi-static respiratory compliance (C st) was calculated by di-viding the V

T

of the pat ient by the corresponding airwa y pressure onthe volume-pressure curve. In each individual patient, the PEEPvalue o f 10 cm H

2

O w as always equal to or greater than Pop.

V

V DA V T 1 P e tCO

2

PaCO

2

( )=

Sta tistical Analysis

Lung dimensions and volumes of upper and lower right a nd left lobeswere compared between patients and healthy volunteers using Stu-dents unpaired t

test. Anteroposterior and cephalocaudal distribu-tions of aerated, poorly aerated, and nonaerated lung parenchyma(expressed in percentage of lobar lung volume) were compared be-tween upper and lower lobes by a two-way analysis of variance for

one grouping and one w ithin factor. The correlation betw een the rest-ing volume of the upper and lower lobes and PEEP-induced alveolarrecruitment a t the lobar level wa s tested by linear regression analysis.The effects of PEEP on hemodynamic and respiratory variables werecompared in nonrecruiter and recruiter patients by a tw o-way ana lysisof variance for one grouping and one within factor. All data are ex-

pressed a s mean

SD . The significance level wa s fixed at 0.05.

RESULTS

Patients

There were 16 male and five female patients (55

17 yr ofage). Ten patients were a dmitted b ecause of complications af-ter surgery: cardiovascular (n

6), orthopedic (n

1), uro-logic (n

1), ma xillofacial (n 1), and neurosurgical (n 1).Nine patients were admitted for multiple trauma, one foracute pancreatitis and one for a ruptured cerebral aneurysm.Seven of the nine patients with multiple trauma had to havesurgery (abdominal surgery, n 1; orthopedic surgery, n 6).Clinical and cardiorespiratory characteristics recorded on theday of inclusion are presented in Tables 1 and 2. The mean de-lay between the onset of A LI and C T scan wa s 5 5 d. Over-all mortality was 38%. Mean durations of the stay in the ICUand of mechanical ventilation were 39 33 d and 36 22 d,respectively. As a mean, patients were severely hypoxemic,with a PaO 2measured a t F IO 21 and ZE EP of 10460 mm Hgand a true shunt value of 44 13%. Furthermore, they hadpulmonary hypertension (mean pulmonary artery pressure

Figur e 3. Anteroposterior and transverse dimensions of the lungmeasured at zero end-expiratory pressure at the level of the tra-cheal carina in the 10 healthy volunteers and the 21 patients withacute lung injury.

Figur e 4. Distribution (expressed in percentage) of aerated (closedpart of bars), poorly aerated (hatched part of bars), and nonaerated(open part of bars) lung areas along the anteroposterior and thecephalocaudal axis for the overall lung in ZEEP. Each barrepre-sents the lung parenchyma located at a given distance (indicatedin centimeters) from the anterior chest wall or from the pulmonaryapex. Aerated lung decreases and nonaerated lung increases alongthe anteroposterior and cephalocaudal axis.

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[Ppa] 32 11 mm Hg) and increased dead space (39 11%). Septic shock was associated w ith AL I in fo ur pat ients.

There were seven male and three female healthy volun-teers (37 16 yr of a ge). The mean heights and weights of t hepatients and healthy volunteers were similar (173 8 versus1726 cm and 70 8 versus 66 10 kg).

Dimensions of the Thorax

As shown in Figure 1, the cephalocaudal dimensions of rightand left lung were significantly reduced in patients with ALI

as compared with those in healthy volunteers (both p 0.05).In patients with ALI, the ratio of cephalocaudal dimension/body height was 7.9 2.3% on the right and 8.5 2.4% onthe left. I n healthy volunteers, corresponding values were 9.82.3% and 11.0 0.7% (both p 0.01). This finding is illus-trated in Figure 2, which shows sagittal CT reconstruction ofthe right lungs of a patient and of a healthy volunteer. Cepha-locaudal dimensions were similar in patients with (148 21and 157 19 mm for the right and left lung, n 6) and with-out (142 27 and 155 28 mm, respective ly, n 15) a surgi-cal thoracic or abdominal incision. As shown in Figure 3, an-teroposterior and transverse diameters of the lung measuredat t he level of the tracheal carina were not different in patientswith ALI from those in healthy volunteers.

Loss of Lung Volume in ZEEP Conditions

Total lung volume (gas plus tissue) in ZEEP of patients withALI was reduced by 27% as compared with healthy volun-

Figur e 5. Distribution (expressed in percentage) along the antero-posterior and cephalocaudal axis of aerated (closed part of bars),poorly aerated (hatched part of bars), and nonaerated (open part ofbars) lung areas of upper and lower lobes analyzed separately.Each barrepresents the lung parenchyma located at a given dis-tance (indicated in centimeters) from the anterior chest wall orfrom the pulmonary apex. Aerated lung areas are mainly locatedin the nondependent regions, whereas nonaerated lung areas arelocated in dependent regions. Between the fourth and the four-teenth centimeter from the anterior chest wall, percentage of eachzone is similar in upper and lower lobes. No cephalocaudal gradi-ent of aerated and nonaerated lung is observed for both upperand lower lobes. For a given distance from the pulmonary apex,

percentage of nonaerated lung areas is always greater and per-centage of aerated lung areas smaller in lower than in upper lobes.

Figur e 6. Percentage of PEEP-induced alveolar recruitment of agiven nonaerated area according to its location on the anteropos-terior (upper panel) and cephalocaudal axis (lower panel) for theupper lobes (open circles) and the lower lobes (closed circles). Thedashed lineindicates the cut-off between PEEP-induced alveolar re-cruitment and derecruitment. PEEP-induced alveolar recruitmentpredominantly occurs in nondependent and cephalad lung re-gions.

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teers (2,777 1,001 ml versus 3,793 647 ml, p 0.01). Vol-ume of pleural fluid was 287 300 ml. As shown in Figure 1,left upper and lower lobes were significantly smaller than thecorresponding right lobes (p 0.001). Resting volumes of up-per lobes were significantly greater than resting volumes oflower lobes (p 0.0001). The reduction in the overall lungvolume and in the volume of lower lobes was similar in pa-tients with a lung injury severity score (LISS) below andabove 2.5. When considering only normally and poorly aer-at ed lung areas, volumes of upper and low er lobes were 83 and17% of the corresponding volumes measured in healthy vol-unteers. When considering both lungs, 31 27% of the lungparenchyma was normally aerated, 36 23% was poorly aer-at ed, and 3314% was nonaera ted.

The distribution of the percentage of aerated, poorly aer-ated, a nd nonaerated lung areas a long the anteroposterior andthe cephalocaudal axis is shown in Figure 4. Aerated lung ar-eas were predominantly located in the most anterior andcephalad regions, whereas nonaera ted lung areas were located

in the most posterior and caudal regions. The distribution ofgas and tissue along the anteroposterior and cephalocaudalaxis for upper and lower lob es analyzed separa tely is shown inFigure 5. The increase in the percentage of nonaerated lungalong the anteroposterior axis was similar between upper andlower lobes. For a given distance from the pulmonary apex,the proportion of a erated lung was always lower and the pro-portion of nonaerated lung was always higher in lower than inupper lobes. For both upper and lower lobes, no cephalocau-dal gra dient in the distribution of gas and tissue was observed,suggesting that upper lobes remain better aerated than dolower lobes, essentially because of their nondependent ana-tomic situat ion.

Factors Influencing PEEP-induced Alveolar Recruitment

As shown in Figure 6, PEEP-induced alveolar recruitment inupper and lower lobes depended on an anteroposterior gradi-ent and was predominantly observed in nondependent lungregions. In the most dependent parts of the lung, the amountof nonaerated tissue increased with PEEP, suggesting aPE EP -induced a lveolar derecruitment. A cephalocaudal gra-dient of PEEP-induced alveolar recruitment was also ob-served in lower lobes, the most cephalad regions recruitingbetter tha n the caudal regions. D erecruitment wa s observed inlung regions that were the closest to the diaphra gmatic cupola.

As shown in Figure 7, a significant correlation was foundbetween the resting volume of the right and left lower lobesand P EE P-induced lobar alveolar recruitment (p 0.001). Asillustrated in Figures 8 and 9, the higher the resting volume oflower lobes, the higher was the PEEP-induced alveolar re-cruitment.

Effects of PEEP-induced Alveolar Recruitment onCardiorespiratory Paramete rs

Pa tients were classified into two groups according to the exist-ence ( recruiter ) or the absence ( nonrecruiter ) of PE EP -induced a lveolar recruitment o n spiral CT scan. P EE P-inducedalveolar recruitment could be demonstrated in 13 patients.

Resting volumes of lower lobes (gas plus tissue) were signifi-cant ly higher in recruiter tha n in nonrecruiter pa tients (1,074492 ml versus 699 125 ml, p 0.01), whereas resting vol-umes of upper lobes were similar between groups (1,965956versus 1,649 318 ml; NS). Respiratory parameters of bothgroups are summarized in Table 3. In nonrecruiters, PEEPhad no effect on Pa O 2, SvO2, PvO2, S/ T, O 2, O2, P E TCO 2,Pa C O2, and D A/VT. In recruiters, PEEP significantly in-creased P a O2 (51 45%), and significantly decreased S/ T(1414%). PE E P increased right atrial pressure and capil-lary wedge pressure in both groups. PEEP had no effect onheart rate, cardiac output, mean arterial pressure, mean pul-monary artery pressure, or systemic and pulmonary vascularresistance.

DISCUSSION

This study demonstrates three original findings. In patientswith severe acute lung injury: (1) there is a reduction of over-all lung volume (gas plus tissue) predominating in the lowerlobes; (2) nonaerated lung regions are distributed not onlyalong an anteroposterior axis, as previously shown (9), butalso along a cephalocaud al axis; (3) in lower lobes, alveolar re-cruitment induced by a PE E P level of 10 cm H2O is correlat edwith the resting volume and decreases along the cephalocau-dal axis. These results were observed in patients showing thecharacteristic features of severe respiratory failure, i.e., lowrespirat ory compliance, marked hypoxemia, increased pulmo-

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Figur e 7. Correlation between the resting volume in ZEEP- andPEEP-induced changes in the volume of nonaerated lung paren-chyma of right lower lobes (upper panel, closed circles) and of leftlower lobes (lower panel, open circles) from the 21 patients. Bothcorrelations were significant (p 0.001). The horizontal dashedlineindicates the cutoff between recruitment and derecruitment.

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nary artery pressure, and alveolar dead space. Nearly twothirds of the patients had a LISS equal or above 2.5, and thevast majority of them had a Pa O2/FIO 2rat io below 200 mm Hg.In addition, the mortality rate was 38%, and the mean dura-tion of mechanical ventilation exceeded 1 mo.

Reduction of FRC (aerated lung volume) is a very commonfinding in patients with the acute respiratory distress syn-drome (1517). An accurate assessment of overall lung vol-ume loss (aerated and nonaerated lung volume) requires to-modensitometric measurements. A single CT section obt ained

Figur e 8. CT scan of a nonrecruiter patient (Patient 14) showing a marked reduction in the volume oflower lobes and no alveolar recruitment with PEEP. The black linerepresents the position of the major fis-sura. The hat ched areasrepresent the pleural fluid. The characteristics of this patient are shown in Tables 1and 2.

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with a conventional scanner allows a bidimensional assess-ment of lung dimensions along the anteroposterior and trans-verse axis and t he measurement of a very small fra ction of thelung vo lume (6, 8, 10, 18, 19). Multiple a nd co ntiguo us CT sec-tions obtained during a short apnea with a spiral CT scanner

offer a tridimensional approach of lung dimensions includingthe cephalocaudal axis. It also allows the measurement of theentire lung volume and the assessment of regional volumes.U sing the tomod ensitometric ana lysis, we found, in healthyvolunteers lying supine, a mea n end-expiratory lung volume of

Figure 9. CT scan of a recruiter patient (Patient 21) showing no reduction in the volume of lower lobes anda marked alveolar recruitment with PEEP. The black linerepresents the position of the major fissura. Thehat ched areasrepresent the pleural fluid. The characteristics of this patient are shown in Tables 1 and 2.

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along t he ant eroposterior axis, which in turn causes compres-sion atelectasis of the dependent lung regions through a de-crease in the transpulmonary pressure. To support their hy-pothesis, they demonstrated that superimposed hydrostaticpressure increases according to a n ant eroposterior gradient inpatients with acute lung injury (9). Further confirmation wasobtained by Sandiford and colleagues (29) who found an in-crease in the radiologic density along an anteroposterior gra-dient in pat ients with acute lung injury although t he increasedpulmonary vascular permeability assessed by positron emis-sion tomography wa s evenly distributed. E xperimentally, oleic-acid-induced lung injury was also shown to induce a depen-dent increase in lung density in dogs (30). We found an in-crease in lung tissue density not o nly along a n ant eroposterioraxis, but also along a cephalocaudal axis. Contrasting with theanteroposterior dependency, cephalocaudal dependency wasobserved on the overall lung but not on upper or lower lobeswhen they were analyzed separately. This difference suggeststhat, besides the decrease in transpulmonary pressure causedby an increased abd ominal pressure, an ana tomic factor is alsoimplicated in t he cephalocauda l distribution of lung hyperden-sities.

PEEP of 10 cm H 2O significantly increased PaO 2, and de-creased S/ Tonly in patients demonstrating scanographic al-

veolar recruitment. The present study supports the findings ofG att inonis group that in acute lung injury, P EE P -induced al-veolar recruitment decreases along the anteroposterior axis,the nondependent parts of the lung recruiting more than thedependent parts. In this respect, upper and lower lobes be-have similarly, the only determinant of PEEP-induced alveo-lar recruitment being the dista nce from the anterior chest wall.We also ob served, similar t o G at tinoni and colleagues (10),that a PEEP of 10 cm H 2O slightly increased the amount ofnoninflated tissue in the most dependent parts of the lung,suggesting that PEEP may be associated with alveolar dere-cruitment related to local compression atelectasis by overdis-tended upper lobes. In lower lobes, PEEP-induced alveolarrecruitment decreased along the cephalocaudal axis. Two CT

scan studies have recently shown that, besides gravity, ate-lectasis secondary to anesthesia also depends upon a cephalo-caudal gradient, the caudal regions being more atelectaticthan the cephalad regions (31, 32). In the present study,PEEP-induced alveolar recruitment in lower lobes was lin-early correlated with resting volume of lower lobes, whereassuch a correlation w as not observed in upper lobes. The open-ing pressure of a passively collapsed lung when transpulmo-nary pressure is zero is known to be near 30 cm H2O (33), apressure much higher than the pressure required to o vercomethe pressure gradient along the anteroposterior axis that wascalculated at 11 cm H 2O by Pelosi and colleagues (9). Passivecollapse of lower lobes related to a diminution of juxtadia-phragmatic transpulmonary pressure likely results in an in-crease in regional opening pressure, which precludes any sig-nificant PE E P-induced alveolar recruitment. Thirty percent ofpatients with acute lung injury do not respond to PEEP (34)or even deteriorate after PEEP implementation (34, 35). Onepossible explanation for the unforeseeable effect of PEEPmight be related to the amo unt of passive atelectasis that is as-sociated with acute respiratory failure. According to our data,the resting volume of t he lower lob es markedly influences theresponse to PEEP.

In conclusion, this study has demonstrated that the markedreduction of lung volume observed in acute lung injury pre-dominat es in lower lobes and influences PE E P -induced alveo-lar recruitment. R eduction in lung volume increases along theanteroposterior and the cephalocaudal axis, suggesting two

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causative mechanisms: an increase in lung weight related toacute lung injury and a passive collapse of low er lobes associ-ated with an upward shift of the diaphragm related t o muscleparalysis and an increase in intra-abdominal pressure. As aconsequence, PEEP-induced alveolar recruitment predomi-nantly o ccurs in nondependent a nd cephalad lung regions.

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