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Am J Respir Crit Care Med Vol 163. pp 16091613, 2001Internet address: www.atsjournals.org

Both reduction in tidal volume (V T) and alveolar recruitment maybe important to limit ventilator-associated lung injury during me-chanical ventilation of patients with the acute respiratory distresssyndrome (ARDS). The aim of this study was to assess the risk of alveolar derecruitment associated with V T reduction from 10 to 6ml/kg. Whether this V T-related derecruitment could be reversed,either by a recruitment maneuver or by an increase in positiveend-expiratory pressure (PEEP) level, was also investigated. Fif-teen patients with ARDS were successively ventilated using con-ventional V T (CVT

10

1 ml/kg) and low V

T

(LV

T

6

1 ml/kg); total PEEP (PEEPtot) was individually set at the lower inflec-tion point (Plip) of the pressure-volume curve (PEEPtot

11

4cm H

2

O). Pressure-volume curves were recorded from zero PEEP(ZEEP) and from PEEP, and recruited volume (Vrec) was calculated

as the volume difference between the two curves for a given pres-sure. Despite a similar PEEPtot, Vrec was significantly lower withLV

T

than with CV

T

, indicating low V

T

-induced alveolar derecruit-ment. Reduction in V

T

was associated with a reduced Sa

O2

. In 10patients, Vrec was also measured before and after a recruitmentmaneuver (two sustained inflations at 45 cm H

2

O), and after an in-crease in PEEP (by 4 cm H

2

O). Low V

T

-induced derecruitment wasreversed by a recruitment maneuver and by increasing PEEP. Weconclude that a reduction in V

T

could be responsible for alveolarderecruitment, which may be transiently reversed by a reexpan-sion maneuver or prevented by a PEEP increase above Plip.

Injury caused by or associated with mechanical ventilation(MV) in acute respiratory distress syndrome (ARDS) has be-come a subject of great concern (1). Various experimental

studies have described the physiologic mechanism by whichMV may lead to ventilation-induced lung injury (VILI) (2, 3).The factors that mainly contribute to VILI include high dis-tending transalveolar pressure or overdistension, related tohigh pressures and volumes that occur at the end of inspira-tion (4), and transalveolar pressure falling below the criticalclosing pressure of alveolar units at the end of expiration, in-ducing repetitive opening-closing phenomenon (3, 5, 6). Al-though these factors occur either at high lung volume (i.e.,overdistension) or at low lung volume (i.e., opening closing),they are often associated throughout the respiratory cycle inthe ARDS lung because of the uneven distribution of lung dis-ease.

On the basis of these clinical and experimental factors, it isnow recommended that, in order to limit VILI, plateau pres-sure should be kept below 30 to 35 cm H

2

O while maintainingthe lung open with sufficient positive end-expiratory pressure(PEEP) (7). Reduction of tidal volume (V

T

) is the cornerstone

of this strategy, and PEEP should be set at a sufficient level inorder to avoid end-expiratory collapse.

Three recent controlled trials that compared low (6 to 8ml/kg) versus conventional (10 to 11 ml/kg) V

T

for a givenPEEP level set empirically, failed to demonstrate any benefitof a pressure-limited strategy with regard to morbidity andmortality (810). In contrast, two other studies showed a sig-nificant benefit on mortality by reducing V

T

(11, 12). One of these studies associated the reduction in V

T

to a high PEEPlevel, whereas the most recent and largest trial to date hasused a high respiratory rate in the low V

T

group, which couldlead to gas trapping and a higher total PEEP. In addition, a re-cent clinical trial demonstrated that the use of high PEEP andlow V

T

reduced inflammatory cytokines level both at the bron-choalveolar lavage and in the blood (2). As previously sug-gested, a high PEEP level could be particularly important inthis low V

T

strategy, because hypoventilation may lead to pro-gressive derecruitment. For this reason, it has been proposedto add recruitment maneuvers to the standard approach of re-duced V

T

(12).The aim of this study was to test the hypothesis that, for a

total PEEP kept constant at the lower inflection point (Plip)on the pressure-volume (Pel-V) curve of the respiratory sys-tem, a reduction in V

T

from 10 to 6 ml/kg could be responsiblefor alveolar derecruitment. The respective efficacy of a re-cruitment maneuver and an increase in PEEP level above Plipwas also assessed by means of the Pel-V curve.

METHODS

Patients

Patients requiring MV for more than 24 h and fulfilling the criteria foracute lung injury as defined by a Pa

O

2

/F

IO

2

ratio

300 mm Hg, bilat-eral opacities on chest radiograph, and no history suggesting elevatedleft atrial pressure, were candidates for inclusion (13). Patients pre-senting with a documented history of chronic obstructive pulmonarydisease or a contraindication for sedation and paralysis were not in-cluded in the study. The protocol was approved by the Henri MondorHospital Ethics Committee, and informed consent was obtained frompatients next of kin.

Fifteen consecutive patients were enrolled in the study. All patientswere sedated, paralyzed, and ventilated in the volume-controlledmode (Servo Ventilator 900C; Siemens-Elema AB, Solna, Sweden).

Pel-V Curve Recording

The system, including a computer-controlled Servo Ventilator 900C,and the technique for performing Pel-V curves, based on the low-flowinsufflation method, have been previously described in detail (14).This allowed Pel-V curves to be obtained either from PEEP or fromzero end-expiratory pressure (ZEEP).

Each Pel-V curve was analyzed according to a mathematical modelthat divided the curve into three segments, separated by a lower andupper inflection point (LIP and UIP, respectively) (15). (

See

onlinedata supplement.)

Alveolar RecruitmentPEEP Pel-V curve was plotted on the same volume axis as the ZEEPPel-V curve, using PEEP-related end-expiratory lung-volume varia-

(

Received in original form April 18, 2000 and in revised form February 6, 2001

)Correspondence and requests for reprints should be addressed to Dr. LaurentBrochard, Ranimation Mdicale, Hpital Henri Mondor, 94010 Creteil, France.E-mail: laurent.brochard@hmn.ap-hop-paris.fr This article has an online data supplement, which is accessible from this issuestable of contents online at www.atsjournals.org

Influence of Tidal Volume on Alveolar Recruitment

Respective Role of PEEP and a Recruitment Maneuver

JEAN-CHRISTOPHE RICHARD, SALVATORE M. MAGGIORE, BJORN JONSON, JORDI MANCEBO, FRANCOIS LEMAIRE,and LAURENT BROCHARD

Medical Intensive Care Unit and INSERM U 492, Henri Mondor Hospital, University Paris XII, Crteil, France

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tion measured during the passive expiration from PEEP to ZEEP.PEEP-related recruitment was defined, for a given elastic pressure(Pel), by the volume difference between both curves, taking into ac-count intrinsic PEEP (PEEPi) (14). This volume represented thePEEP-related recruitment of previously collapsed lung units, and wasidentified by the upward shift along the volume axis of the PEEP Pel-V curve, relative to the ZEEP Pel-V curve. Recruitment could bequantified at any elastic pressure studied.

Protocol

The first Pel-V curve was obtained from ZEEP, without modifyingprevious ventilator settings, in order to determine pressure at the LIP(Plip). The total PEEP (PEEPtot) level (taking into account PEEPi)was set close to Plip and kept constant whatever the V

T

tested, by

modifying external PEEP level when necessary. The respiratory rate(from 18 to 22 min

1

), the inspiratory/total time ratio (0.33), and theF

IO

2

were also kept constant.

First part of the study (15 patients).

Patients were successively ven-tilated with conventional V

T

(CV

T

10 ml/kg of dry body weight)and low V

T

(LV

T

6 ml/kg) randomly applied. Patients were venti-lated 1 h in each mode. After sampling blood for arterial blood gasmeasurements, the following measurements were made during thelast 10 min of each condition (CV

T

and LV

T

). (

1

) The PEEP Pel-Vcurve was recorded after a prolonged expiration during which PEEPwas maintained. (

2

) The ZEEP Pel-V curve was then recorded after aprolonged expiration during which PEEP was eliminated (i.e., fromthe elastic equilibrium volume reached at ZEEP).

Second part of the study (10 patients).

Similar measurements weremade, respectively, with CV

T

and LV

T

immediately after two succes-sive recruitment maneuvers consisting of a 45 cm H

2

O pressure-lim-

ited breath applied for 15 s.

Third part of the study (10 patients).

The PEEP level was then in-creased by 4 cm H

2

O, taking into account PEEPi to keep PEEPtotconstant whatever the V

T

. Pel-V curve recordings and recruitmentcalculation were repeated after 1 h of CV

T

and LV

T

ventilation com-bined with the high level of PEEP.

Statistics

Values are given as means

SD. At a given PEEP level, alveolar re-cruitment (calculated for any given Pel), ventilatory settings, hemody-namic data, and arterial blood gases measured with CV

T

and LV

T

,were compared using Wilcoxons test for paired samples. The effect of a recruitment maneuver and increasing PEEP was compared withthose observed before recruitment maneuver or PEEP increase usingthe same test. Significant differences were considered for p

0.05.

RESULTS

Arterial blood gases and Pel-V curves recorded from PEEPset at Plip, and from ZEEP, were obtained in 15 patients withCV

T

and LV

T

, respectively. The mean LIP was 10

4 cmH

2

O. Pel-V curves were also recorded after a recruitment ma-neuver and after an increase in PEEP by 4 cm H

2

O in 10 pa-tients of the whole population. The characteristics of the pa-tients are presented in Table 1.

Influence of V

T

Keeping PEEP Constant

Both strategies were well tolerated by all patients. Ventilatorysettings, plateau pressure (Pplat), setPEEP, and PEEPtot aregiven in Table 2. PEEPtot observed with CV

T

did not differfrom LV

T

, and this was achieved by individual adaptation of external PEEP level. As expected, Pa

CO 2

was significantlyhigher with LV

T

(Table 3). Hemodynamic parameters werenot affected by change in V

T

(Table 3).Over the Pel range from 15 to 30 cm H

2

O, recruitment wassignificantly higher with CV

T

than with LV

T

, for a similarPEEPtot level. Recruitment calculated for 20, 25, and 30 cmH

2

O of Pel, is illustrated in Figure 1. Expressed as a percent-age of the amount of recruitment observed with CV

T

, recruit-ment with LV

T

was only 69% at 15 cm H

2

O and 59% at 30 cmH

2

O. Pa

O 2

, as well as Pa

O2

/F

IO 2

, were not significantly altered

TABLE 1. PATIENT CHARACTERISTICS

PatientNo.

Age(

yr

) SAPS IIUnderlying

Disease

Cause of AcuteRespiratory

Failure

LungInjuryScore

P/F(

mm Hg

)PEEP

(

cm H

2

O)

DaysReceiving

MV Outcome

1 51 54 Esophagealneoplasm

Aspiration 2.5 204 6 3 S

2 30 54 Lupus Pneumonia 3.5 247 12 3 S3 41 25 Cirrhosis Aspiration 3.0 210 14 2 S4 62 49 Cirrhosis Aspiration 2.5 70 14 2 D5 44 36 Pneumonia 2.8 90 12 2 S6 42 26 Multiple

trauma Aspiration 3.3 150 5 3 D

7 77 41 Cardiacsurgery

Pneumonia 3.0 102 8 3 D

8 34 20 Pneumonia 3.0 165 10 2 S9 60 56 Ischemic

cardiopathyPneumonia 2.5 177 14 7 D

10 46 41 Septic shock 2.8 190 8 6 S11 24 33 Septic shock 2.8 244 12 1 D12 66 49 Epilepsy Pneumonia 2.5 80 8 2 S13 78 60 Pneumonia 2.3 153 5 2 S14 76 78 Cirrhosis Pneumonia 3.3 120 10 3 S15 29 37 Aspiration 2.3 100 5 2 S

Definition of abbreviations

: D

died; MV

mechanical ventilation; PEEP

positive end-expiratory pressure; P/F

Pa

O2

/F

I

O2

ratio; S

survived; SAPS II

simplified acute physio-logic score II.

TABLE 2. VENTILATORY SETTINGS DURING VENTILATION WITHPEEP SET AT Plip*

LV

T

(

n

15)CV

T

(

n

15) p Value

V

T

, ml 411

55 664

84

0.01 V

T

, ml kg

1

6

1 10

1

0.01setPEEP, cm H

2

O 10

4 10

4 NSPEEPtot, cm H

2

O 11

4 11

4 NSPplat, cm H

2

O 23

8 30

10

0.01

Definition of abbreviations

: CV

T

conventional tidal volume; LV T low tidal volume;NS not significant; PEEPtot total end-expiratory pressure; Plip lower inflectionpoint of pressure-volume curve; Pplat plateau pressure; setPEEP external end-expi-ratory pressure; V T tidal volume.

* All results are presented as mean SD. p Value indicates the significant difference between LV T and CV T.

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by reduction of V T. SaO 2 was significantly lower with LV T thanwith CV T (Table 3).

Effect of a Recruitment Maneuver on the DerecruitmentInduced by Low V T

In the 10 patients in whom a recruitment maneuver was per-formed, PEEPtot set at LIP and Pplat were: 13 3 versus 134 cm H 2O, NS, and 36 7 versus 28 7 cm H 2O, p 0.01, forCV T and LV T, respectively. The comparison of recruitmentbetween CV T and LV T before the recruitment maneuvershowed the same difference as in the 15 patients.

With LV T, a recruitment maneuver induced a significantincrease in recruitment (175 108 ml versus 254 137 ml, ex-pressed at a Pel of 20 cm H 2O, p 0.01). In contrast, the samerecruitment maneuver did not significantly affect recruitmentwith CV T (266 157 ml versus 264 120 ml, NS). As a result,PEEP-induced recruitment became similar for LV T and CV Tafter the recruitment maneuver (Figure 1).

Effect of Increasing PEEP on the DerecruitmentInduced by Low V T

In the same 10 patients, the 4 cm H 2O increase in PEEP modi-fied PEEPtot and Pplat to 17 3 versus 16 3 cm H 2O, NS,and to 41 9 versus 32 7 cm H 2O, p 0.01 for CV T andLV T, respectively.

The increase in PEEP induced an increase in recruitmentfor both V T (expressed at 20 cm H 2O of Pel: 175 108 versus332 91 ml with LV T, p 0.05, and 266 157 versus 464216 ml with CV T, p 0.05) (Figure 1). At this high PEEP

level, the difference in recruitment between LV T and CV T(Figure 1) did not reach significance.

DISCUSSION

The present study has demonstrated that a reduction in V Tfrom 10 to 6 ml/kg, keeping PEEPtot constant at the LIP, wasresponsible for a significant lung volume loss corresponding toalveolar derecruitment. This effect may have participated, atleast in part, to the negative results of three recent clinical tri-als that failed to demonstrate any benefit of a ventilatory strat-egy aiming at systematically reducing V T (810). This hypoth-esis is corroborated by the significant reduction in mortalityrate associated with a lung protective strategy recently re-ported by Amato and colleagues (12). In this study, particularattention was given to the PEEP setting, as well as to repeatedsighs, performed to preserve lung recruitment during low V Tventilation. In contrast, the recent NIH Network trial seems toindicate that reduction in V T alone is effective to reduce mor-tality. However, the possibility of a PEEPi effect in the low V Tgroup, caused by the high respiratory frequencies used, makesthe interpretation of these results still open.

The apparent conflicting results of these recent clinical tri-als could also suggest that, first, reduction in V T from 10 to 6

ml/kg alone fails to improve mortality and, second, that a spe-cific strategy to avoid harmful alveolar derecruitment may bebeneficial. In addition, a recent clinical study has indicatedthat a low PEEP associated with high V T may lead to systemicinflammatory response and possibly promotes lung injury (2).

Alveolar DerecruitmentSeveral studies based on CT scan, Pel-V curves, or gas ex-change have demonstrated that recruitment is a continuous andprogressive phenomenon that not only depends on PEEP butalso on peak inflation volume (14, 1618). Considering a givenPEEP level, if tidal inflation induces recruitment, a reductionin V T could thus be responsible for alveolar derecruitment. Ithas been demonstrated that low V T ventilation during anes-

thesia could be responsible for alveolar collapse in healthylungs (19, 20). Several factors, including the use of high F IO 2 inthe presence of low / ratio, the use of low V T, sedation, andparalysis may facilitate atelectasis and promote denitrogena-tion atelectasis in patients with ARDS (2123). Cereda andcolleagues (24) have shown that low V T ventilation could in-duce a progressive decrease in compliance, indicating a time-dependent derecruitment, which could be prevented by higherPEEP level. The influence of V T on PEEP-related cardiore-

V Q

TABLE 3. GAS EXCHANGE AND HEMODYNAMIC PARAMETERSDURING VENTILATION WITH PEEP SET AT Plip*

LV T(n 15)

CV T(n 15) p Value

PaO2, mm Hg 136 80 154 82 NSPaO2/FIO2, mm Hg 165 84 183 80 NSSaO2, % 94.8 5.0 97.6 2.1 0.05PaCO2, mm Hg 60 35 38 21 0.001pH 7.21 0.1 7.36 0.1 0.001SBP, mm Hg 125 25 121 20 NSDBP, mm Hg 60 9 60 10 NSHR, min 1 101 15 93 15 NS

Definition of abbreviations : CV T conventional tidal volume; DBP diastolic bloodpressure; HR heart rate; LV T low tidal volume; NS not significant; SBP systolicblood pressure.

* All results are presented as mean SD. p Value indicates the significant difference between LV T and CV T.

Figure 1. Alveolar recruitment, measured as the volume differ-ence between pressure-volume curves traced from PEEP and fromZEEP, expressed over the range of distending pressures (Pel) whereboth curves are traced during low tidal volume (LV T) and con-ventional tidal volume (CV T), respectively, and using the samePEEP level. Values are expressed as means and standard devia-tions. On the left, the baseline PEEP level set at the lower inflec-tion point (LIP) is used; in the middle, the same measurementsare performed immediately after a recruitment maneuver; onthe right, PEEP has been increased by 4 cm H 2O. Significant dif-

ferences between CV T and LV T were found only in the first situa-tion. *Indicates significant difference (p 0.05) between LV Tand CV T; **p 0.01.

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spiratory effect was also studied by Ranieri and colleagues (25)in a group of nine patients with ARDS. Recruitment based onPel-V curve analysis was measured in each patient during lowand high tidal ventilation for a constant PEEP level. In allpatients, the Pel-V curve from ZEEP during low V T ventila-tion exhibited a concavity toward the volume axis, which sug-gested a recruitable lung, whereas the Pel-V curves recordedwith high V T were convex in six patients, indicating a progres-sive decrease in compliance suggesting overdistension. Theseinvestigators concluded that with high V T, PEEP mainly in-duced hyperinflation of alveoli already recruited by tidal ven-tilation, whereas with low V T, PEEP induced alveolar recruit-ment and counterbalanced low V T-related derecruitment.Despite some discrepancies with our results, possibly relatedto methodologic differences, the results reported by Ranieriand colleagues showed that low V T ventilation might affectlung recruitment. A recent study corroborating these findingssuggested that the size of V T might interfere with recruitmentby modifying the behavior of airway resistance and time con-stant (26). In the present study, the significant alveolar dere-cruitment associated with V T reduction was recovered by in-creasing PEEP, which confirmed that the lung was not fullyrecruited during low V T ventilation. However, because we keptVT constant at the two different PEEP levels (either with LV Tor with CV T), the Pplat increased with the higher PEEP level.Therefore, we cannot determine whether the greater recruit-ment was a result of the Pplat causing inflation of more lungunits at end-inspiration or higher PEEP preventing more timedependent end-expiratory collapse or both.

Influence on OxygenationIt is known that oxygenation depends on recruitment, and there-fore a worsening in oxygenation could have been expectedwith low V T. In the present study, Pa O2 did not significantlychange with the reduction in V T but arterial oxygen satura-tion worsened. A right-shift in the oxyhemoglobin dissociationcurve caused by acidosis may have participated to this latterfinding. However, the influence of V T reduction on gas ex-

change remains controversial in the studies that have specifi-cally addressed this issue. Several mechanisms, not directly re-lated to recruitment, could be involved in the oxygenationchanges occurring after V T reduction. Hypercapnia associatedwith V T reduction tends to increase cardiac output (2729).This effect may improve Pa O 2 by increasing mixed venous oxy-gen saturation or decrease Pa O 2 by increasing shunt. In thestudy reported by Ranieri and colleagues (26), Pa O 2 was signif-icantly improved when V T was reduced from 12 to 7 ml/kg.These results greatly differ from those of Blanch and colleagues(30) who reported a better recruitment as well as a Pa O 2 im-provement associated with an increase in V T. In this study,minute ventilation was matched by increasing respiratory ratewith low V T in order to limit hypercapnia induced by V T re-duction. Kiiski and colleagues (31, 32) studied the influence of VT on gas exchange and oxygen delivery during, respectively,nonmatched and matched minute ventilation. Both studies sug-gested that changes in gas exchange observed with low V T notonly depend on recruitment but also on the hemodynamic ef-fects associated with hypercapnia. Our results concerning oxy-genation should be interpreted with caution because of therelatively small number of patients. The absence of invasivehemodynamic monitoring makes it difficult to interpret the ef-fects of both ventilatory strategies on oxygenation.

Recruitment ManeuverThe lung protective approach reported by Amato and col-leagues (12) included the application of systematic sighs after

tracheal suctioning, with the aim of avoiding harmful alveolarcollapse. The rationale for using a recruitment maneuver is toforestall collapsed lung units, which suggests that this tech-nique is effective when the lung has previously been dere-cruited. Several studies have demonstrated the effect of sighson atelectasis observed during general anesthesia (19, 20).Pelosi and colleagues (33) investigated the effects of sighs ongas exchange in patients with acute lung injury. These investi-gators demonstrated that application of sighs during lung pro-tective strategy could improve lung volume and oxygenation.These results indicate that a low V T strategy may not providefull lung recruitment despite the relatively high PEEP level(14 2 cm H 2O) applied. A recent study confirmed these find-ings but also suggested that recruitment maneuvers were lessefficient than PEEP increase (34). In our study, the increase inrecruitment resulting from the recruitment maneuver was ob-served only during low V T ventilation. Interestingly, the samemaneuver did not lead to any significant beneficial effect dur-ing CV T ventilation, indicating that the lung remained openand therefore was no longer recruitable. However, time effectof recruitment maneuver could not be evaluated since ventila-tory settings were changed to higher PEEP level immediatelyafter measurements.

In conclusion, the most relevant finding of this study wasthat a ventilatory strategy based on recent recommendations(i.e., limited V T and PEEP at or above Plip) leads to alveolarinstability and lung collapse. These results suggest that a spe-cific approach may be needed to prevent alveolar instability inthe situation where strategies limiting end-inspiratory pres-sure and overdistension are used. In our study, increasingPEEP or performing a recruitment maneuver appear as twopossible strategies to counteract low V T-induced derecruit-ment.

Acknowledgment : The writers thank Richard Medeiros for his help in edit-ing the manuscript, Lucie Breton for technical support during the study,and Florence Picot for her help in typing the manuscript.

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