ORIGINAL ARTICLE

Diaphragm ultrasound as a predictor of successfulextubation from mechanical ventilationErnest DiNino, Eric J Gartman, Jigme M Sethi, F Dennis McCool

Memorial Hospital of RhodeIsland and Brown University,Pawtucket, Rhode Island, USA

Correspondence toDr F Dennis McCool,Pulmonary, Critical Care andSleep Medicine, MemorialHospital of Rhode Island andBrown University, Pawtucket,RI 02860,USAF_McCool@Brown.edu

Received 2 July 2013Revised 20 November 2013Accepted 27 November 2013Published Online First23 December 2013

http://dx.doi.org/10.1136/thoraxjnl-2013-204920

To cite: DiNino E,Gartman EJ, Sethi JM, et al.Thorax 2014;69:423427.

ABSTRACTIntroduction The purpose of this study was toevaluate if ultrasound derived measures of diaphragmthickening, rather than diaphragm motion, can be usedto predict extubation success or failure.Methods Sixty-three mechanically ventilated patientswere prospectively recruited. Diaphragm thickness (tdi)was measured in the zone of apposition of the diaphragmto the rib cage using a 710 MHz ultrasound transducer.The percent change in tdi between end-expiration andend-inspiration (tdi%) was calculated during eitherspontaneous breathing (SB) or pressure support (PS)weaning trials. A successful extubation was dened as SBfor >48 h following endotracheal tube removal.Results Of the 63 subjects studied, 27 patients wereweaned with SB and 36 were weaned with PS. Thecombined sensitivity and specicity of tdi%30% forextubation success was 88% and 71%, respectively. Thepositive predictive value and negative predictive valuewere 91% and 63%, respectively. The area under thereceiver operating characteristic curve was 0.79 for tdi%.Conclusions Ultrasound measures of diaphragmthickening in the zone of apposition may be useful topredict extubation success or failure during SB or PS trials.

INTRODUCTIONTiming is critical when determining if a patient canbe successfully extubated. Premature discontinuationof mechanical ventilation may lead to increased car-diovascular and respiratory stress, CO2 retention andhypoxaemia with up to 25% of patients requiringreinstitution of ventilator support.1 2 Unnecessarydelays in weaning from mechanical ventilation alsocan be deleterious. Complications such as ventilatorassociated pneumonia and ventilator induced dia-phragm atrophy can be seen with short periods ofmechanical ventilation thereby prolonging mechan-ical ventilation.36

Tools available for determining the optimaltiming of extubation are limited. Subjective deci-sions are often wrong.7 Stroetz and Hubmayr8

found that clinical prediction of extubation successor failure was often incorrect with the decision toextubate biased toward ventilator dependency.Measures such as breathing frequency (f ), minuteventilation, and negative inspiratory force, havedone little to improve the timing of successful extu-bation.911 A more recent parameter, the rapidshallow breathing index (RSBI) provides a guide fortiming extubation with spontaneous breathing (SB)trials but its value is limited when used to predictsuccessful extubation during pressure support (PS)trials.12 13

Direct measures of diaphragm function as predic-tors of extubation success or failure have not beenextensively evaluated. Motion of the diaphragmdome has been assessed using M mode ultra-sound14 15 and found to be useful in predictingextubation outcomes16 17; however, imaging thedome does not directly visualise the diaphragmmuscle itself and factors such as breath size, imped-ance of neighbouring structures, abdominal compli-ance, rib cage or abdominal muscle activity, andascites will affect regional and global diaphragmmotion of the tendonous dome of the diaphragm.18

This drawback can be circumvented by ultrasonog-raphy of the diaphragm in the zone of apposition(ZAP) as this approach allows for direct visualisa-tion of the diaphragm muscle and assessment of itsactivity.1925 Diaphragm thickening during inspir-ation reects diaphragm shortening and is analo-gous to an ejection fraction of the heart. Thepurpose of this study was to assess whether thedegree of diaphragm thickening as measured by Bmode ultrasound during a weaning trial can beused to predict extubation outcomes.

METHODSSubjectsSixty-three patients were prospectively recruitedfrom medical intensive care units at MemorialHospital of Rhode Island and Rhode IslandHospital. The study was approved by the

Editors choiceScan to access more

free content

Key messages

What is the key question? Can ultrasound measurements of diaphragm

muscle thickening during inspiration provide ameasure of extubation success or failure?

What is the bottom line? We found that measurements of diaphragm

thickening in the zone of appositionoutperform standard measures of extubationoutcome.

Why read on? Learn the rationale for using ultrasound

measures of diaphragm muscle thickening topredict extubation outcomes, how thesemeasures differ from ultrasound measures ofdiaphragm dome motion, and how thismeasure compares with other measures usedto predict extubation success or failure.

DiNino E, et al. Thorax 2014;69:423427. doi:10.1136/thoraxjnl-2013-204111 423

Critical care

group.bmj.com on October 31, 2014 - Published by http://thorax.bmj.com/Downloaded from

institutional review boards at both the institutions (IRB #09-45for Memorial Hospital of Rhode Island and CMTT #0095-10for Rhode Island Hospital) and informed consent was obtainedfor all study participants. All patients were clinically stable andidentied by the intensivist as ready to undergo a low-level PSweaning trial or a SB trial. Subjects were recruited 624 h priorto the rst weaning trial. The ultrasonographer was notied ofthe intensivists decision to start weaning and obtained informedconsent. No specic disease process was required for entry intothe study other than the presence of respiratory failure. All sub-jects had a fraction of inspired oxygen (FIO2) of

to a PS of 5/5 had a median of 5.00 days of ventilator supportwith an IQR of 4.00. The patients weaned with a SB trialreceived a median of 5.00 days of ventilator support with anIQR of 8.50 days.The tdi% and tdi end-expiration values for all subjects are

shown in gures 2A,B respectively. Of the 49 patients who weresuccessfully extubated, 43 had a tdi% of 30%. Of the 14who failed extubation, 10 had a tdi%< 30%. The resultingsensitivity and specicity was 88% and 71%, respectively. ThePPV of a tdi% 30% for extubation success was 91% and theNPV of a tdi < 30% for extubation failure was 63% (table 1).The area under the ROC curve for tdi% was 0.79 (gure 3A)and for tdi end-expiration it was 0.61 (gure 3B).Four patients failed extubation despite having a tdi% 30%.

However, factors unrelated to diaphragm contractility such asthe development of congestive heart failure (CHF), fever andacute change in mental status, mucous plugging, and aspiration,precipitated respiratory failure and the need for reintubation inthese individuals. These non-mechanical factors lowered theNPV and specicity of tdi%. The remaining 10 patients whofailed extubation had a tdi%< 30%. In these individuals extu-bation failure was attributed to respiratory pump failure ineight. One patient failed because of uid overload and fever andone because of a new cerebrovascular accident (CVA) andaspiration.When comparing the subgroups of those weaned using PS

and those weaned with a SB trial, tdi% predicted extubationsuccess or failure equally well. Of the 25 patients who weresuccessfully extubated at a PS of 5/5, 24 had a tdi% 30%.Of the 11 patients who failed extubation, 7 had a tdi%< 30%. The resulting sensitivity, specicity, PPV and NPV arelisted in table 2. Of the 24 patients successfully extubated aftera SBT, 18 had a tdi% 30%. Of the three patients who failedextubation, all had a tdi%< 30%. The resulting sensitivity,specicity, PPV and NPV are listed in table 2. The RSBI wascalculated for 27 patients who underwent a SBT. The sensitiv-ity, specicity, PPV and NPV for a RSBI 105 are given intable 2.We evaluated if measures of tdi at end-expiration or if com-

posite measures of tdi% and breathing pattern would be betterpredictors of successful extubation than tdi% alone (table 1).None of these parameters (tdi at end-expiration, tdi%VT andtdi%/f) enhanced the predictive value of tdi% alone.

DISCUSSIONUltrasound is a technology that is increasingly used by intensivecare physicians to assist in central line placement and other pro-cedures.26 Recently, ultrasound has been used to assess the pres-ence of diaphragm dysfunction postoperatively,27 to identify theoccurrence of ventilator induced diaphragm injury3 and toevaluate diaphragm dome motion during SB weaning trials.16

However, the extent to which the diaphragm dome movesduring inspiration can be affected by breath size, impedance ofneighbouring structures and abdominal compliance. These

Figure 2 Values for (A) tdi%, (B) tdi end-expiration are depicted forall subjects who were successfully extubated or failed extubation. Thedashed line represents the cut-off value for tdi% (30%) and tdiend-expiration ( 0.17 cm).

Table 2 Weaning parameters

Weaning index NumberSensitivity(%)

Specificity(%)

PPV(%)

NPV(%)

Weaning parameters for the PS 5/5 grouptdi% 36 96 64 86 88tdi%VT 36 96 64 86 88tdi atend-expiration

36 84 18 70 33

Weaning parameters for the SB trial grouptdi% 27 75 100 100 67tdi%VT 27 78 100 100 38RSBI 26 87 33 91 25

tdi atend-expiration

27 96 33 92 50

Threshold for RSBI=105 (min/L).NPV, negative predictive value; PPV, positive predictive value; PS, pressure support;RSBI, rapid shallow breathing index; SB, spontaneous breathing; VT, tidal volume.

DiNino E, et al. Thorax 2014;69:423427. doi:10.1136/thoraxjnl-2013-204111 425

Critical care

group.bmj.com on October 31, 2014 - Published by http://thorax.bmj.com/Downloaded from

confounders can be circumvented by visualising the diaphragmmuscle itself in the zone of apposition. The present study indi-cates B mode ultrasound can be used to predict extubation out-comes during PS and SB weaning trials.B mode ultrasound measurements of tdi have been correlated

with diaphragm strength and muscle shortening.19 20 23 Thevolume of diaphragm muscle mass is constant as it contracts.Therefore as it shortens, it thickens and measures of tdi areinversely related to changes in diaphragm length (ldi) (tdi 1/ldi). In support of this notion, calculation of ldi from mea-sures of tdi in healthy individuals are in the range of what hasbeen measured in humans and the absence of diaphragm thick-ening has been noted in patients with diaphragm paralysis.20 28

Since the diaphragm is the major muscle of inspiration, the pres-ence of diaphragm contraction and shortening should be a pre-requisite for successful extubation. The high PPV of tdi%

30% and our nding that 10 of 14 patients who failed extuba-tion had a tdi%

no special effort by the patient, and can be used during eitherPS or SB trials. The ubiquitous presence of ultrasound equip-ment in intensive care units indicates that there need not be add-itional capital equipment expenditures. The portability andavailability of ultrasound make measures of tdi ideally suited forincorporation into the intensivists decision-making process tocomplement the complete assessment of the patient in evaluat-ing extubation outcome.

Contributors FDM is the guarantor of the content of the manuscript, including thedata and analysis. ED has made substantial contributions to acquisition of data,data analysis, data interpretation and drafting the manuscript EJG has madesubstantial contributions to design, data interpretation, and provided critical revisionsfor important intellectual content. JMS has made substantial contributions to design,data interpretation, and provided critical revisions for important intellectual content.

Competing interests None.

Ethics approval Memorial Hospital of Rhode Island IRB and Rhode Island HospitalIRB.

Provenance and peer review Not commissioned; externally peer reviewed.

REFERENCES1 Esteban A, Anzueto A, Frutos F, et al. Characteristics and outcomes in adult

patients receiving mechanical ventilation: a 28-day international study. JAMA2002;287:34555.

2 Funk GC, Anders S, Breyer MK, et al. Incidence and outcome of weaning frommechanical ventilation according to new categories. Eur Respir J 2010;35:8894.

3 Grosu HB, Lee YI, Lee J, et al. Diaphragm muscle thinning in patients who aremechanically ventilated. Chest 2012;142:145560.

4 Hudson MB, Smuder AJ, Nelson WB, et al. Both high level pressure supportventilation and controlled mechanical ventilation induce diaphragm dysfunction andatrophy. Crit Care Med 2012;40:125460.

5 Vassilakopoulos T. Ventilator-induced diaphragm dysfunction: the clinical relevanceof animal models. Intensive Care Med 2008;34:716.

6 Levine S, Nguyen T, Taylor N, et al. Rapid disuse atrophy of diaphragm bers inmechanically ventilated humans. N Engl J Med 2008;358:132735.

7 Ely EW, Baker AM, Evans GW, et al. The prognostic signicance of passing a dailyscreen of weaning parameters. Intensive Care Med 1999;25:5817.

8 Stroetz RW, Hubmayr RD. Tidal volume maintenance during weaning with pressuresupport. Am J Respir Crit Care Med 1995;152:103440.

9 Krieger BP, Ershowsky PF, Becker DA, et al. Evaluation of conventional criteria forpredicting successful weaning from mechanical ventilatory support in elderlypatients. Critical Care Med 1989;17:85861.

10 Nemer SN, Barbas CS, Caldeira JB, et al. Evaluation of maximal inspiratory pressure,tracheal airway occlusion pressure, and its ratio in the weaning outcome. J Crit Care2009;24:4416.

11 Conti G, Montini L, Pennisi MA, et al. A prospective, blinded evaluation of indexesproposed to predict weaning from mechanical ventilation. Intensive Care Med2004;30:8306.

12 Yang KL, Tobin MJ. A prospective study of indexes predicting the outcome of trialsof weaning from mechanical ventilation. N Engl J Med 1991;324:144550.

13 Lee KH, Hui KP, Chan TB, et al. Rapid shallow breathing (frequency-tidal volumeratio) did not predict extubation outcome. Chest 1994;105:5403.

14 Houston JG, Morris AD, Howie CA, et al. Technical report: quantitative assessmentof diaphragmatic movementa reproducible method using ultrasound. Clin Radiol1992;46:4057.

15 Gerscovich EO, Cronan M, McGahan JP, et al. Ultrasonographic evaluation ofdiaphragmatic motion. J Ultrasound Med 2001;20:597604.

16 Jiang JR, Tsai TH, Jerng JS, et al. Ultrasonographic evaluation of liver/spleenmovements and extubation outcome. Chest 2004;126:17985.

17 Kim WY, Suh HJ, Hong SB, et al. Diaphragm dysfunction assessed byultrasonography: inuence on weaning from mechanical ventilation. Critical CareMed 2011;39:262730.

18 Miller WT, Talman EA. Subphrenic abscess. Am J Roentgenol Radium Ther NuclMed 1967;101:9619.

19 Cohn D, Benditt JO, Eveloff S, et al. Diaphragm thickening during inspiration. J ApplPhysiol 1997;83:2916.

20 Gottesman E, McCool FD. Ultrasound evaluation of the paralyzed diaphragm.Am J Respir Crit Care Med 1997;155:15704.

21 Summerhill EM, El-Sameed YA, Glidden TJ, et al. Monitoring recovery fromdiaphragm paralysis with ultrasound. Chest 2008;133:73743.

22 McCool FD, Tzelepis GE. Dysfunction of the diaphragm. N Engl J Med2012;366:93242.

23 McCool FD, Conomos P, Benditt JO, et al. Maximal inspiratory pressures anddimensions of the diaphragm. Am J Respir Crit Care Med 1997;155:132934.

24 McCool FD, Benditt JO, Conomos P, et al. Variability of diaphragm structure amonghealthy individuals. Am J Respir Crit Care Med 1997;155:13238.

25 Rehan VK, Laiprasert J, Wallach M, et al. Diaphragm dimensions of the healthypreterm infant. Pediatrics 2001;108:E91.

26 Matamis D, Soilemezi E, Tsagourias M, et al. Sonographic evaluation of thediaphragm in critically ill patients. Technique and clinical applications. Intensive CareMed 2013;39:80110.

27 Kim SH, Na S, Choi JS, et al. An evaluation of diaphragmatic movement by M-modesonography as a predictor of pulmonary dysfunction after upper abdominal surgery.Anesth Analg 2010;110:134954.

28 Rochester DF, Farkas GA, Lu J. Contractility of the in situ diaphragm: assessmentbased on dimensional analysis. Respiratory Muscles and their Neuromotor Control:Proceedings of an Iups Satellite Symposium Held in Los Angeles, California,July 2224, 1986. New York: Liss, 1987.

29 Hershenson MB, Kikuchi Y, Tzelepis GE, et al. Preferential fatigue of the rib cagemuscles during inspiratory resistive loaded ventilation. J Appl Physiol1989;66:7504.

30 Hershenson MB, Kikuchi Y, Loring SH. Relative strengths of the chest wall muscles.J Appl Physiol 1988;65:85262.

DiNino E, et al. Thorax 2014;69:423427. doi:10.1136/thoraxjnl-2013-204111 427

Critical care

group.bmj.com on October 31, 2014 - Published by http://thorax.bmj.com/Downloaded from

ventilationsuccessful extubation from mechanical Diaphragm ultrasound as a predictor of

Ernest DiNino, Eric J Gartman, Jigme M Sethi and F Dennis McCool

doi: 10.1136/thoraxjnl-2013-2041112014 69: 431-435 originally published online December 23, 2013Thorax

http://thorax.bmj.com/content/69/5/431Updated information and services can be found at:

These include:

References #BIBLhttp://thorax.bmj.com/content/69/5/431

This article cites 29 articles, 5 of which you can access for free at:

serviceEmail alerting

box at the top right corner of the online article. Receive free email alerts when new articles cite this article. Sign up in the

CollectionsTopic Articles on similar topics can be found in the following collections

(972)Airway biology (133)Mechanical ventilation (140)Mechanical ventilation (608)Radiology (diagnostics)

(95)Editor's choice

Notes

http://group.bmj.com/group/rights-licensing/permissionsTo request permissions go to:

http://journals.bmj.com/cgi/reprintformTo order reprints go to:

http://group.bmj.com/subscribe/To subscribe to BMJ go to:

group.bmj.com on October 31, 2014 - Published by http://thorax.bmj.com/Downloaded from